Iodine status of children and knowledge, attitude, practice of iodised salt use in a remote community in Kerema district, Gulf province, Papua New Guinea

Iodine deficiency is the single most common cause of preventable mental impairment in communities with suboptimal iodine intake. Objective of the present study was to assess in more detail the iodine status and knowledge, attitudes and practice (KAP) relating to use of iodised salt in a remote community in Kotidanga area, Kerema district, Gulf province, Papua New Guinea. This prospective school and community based cross-sectional study was carried out in 2017. Simple random sampling was used to select schools. Multistage sampling was used to randomly select 300 children aged 6 to 12 years, of which 289 consented to participate in the study. A single urine sample was collected from each of the consenting children, as well as a salt sample from their households. Discretionary salt intake was assessed in a sub-sample of the children’s households. Salt iodine content and urinary iodine concentration (UIC) were analysed. A semi-structured modified Food and Agriculture Organisation questionnaire was used to assess KAP of three different community groups. Only 64% of households had salt on the day of data collection. Mean iodine content in household salt samples was 29.0 ± 19.1 ppm. Iodine content was below 30.0 ppm in 54.8% and below 15.0 ppm in 31.2% of salt samples. Mean per capita discretionary intake of household salt was 2.9 ± 1.8 g/day. Median UIC was 25.5 μg/L and Interquartile Range was 15.0 to 47.5 μg/L, indicating moderate status iodine nutrition. Median UIC was 34.3 μg/L for children in households with salt, compared to 15.5 μg/L for children in households without salt, indicating severe iodine deficiency in the latter group. The three community groups had limited knowledge about importance of using iodised salt and consequences of iodine deficiency on health outcomes. This remote community has limited access to adequately iodised household salt due to high cost, inappropriate packaging, storage and food preparation, resulting in iodine deficiency. Strategies to increase iodine intake are needed.


Introduction
Iodine is a trace element required for the biosynthesis of thyroid hormones, which are crucial to growth and development. Low bioavailability or deficiency of iodine may lead to a spectrum of disorders called iodine deficiency disorders (IDD) [1,2]. This may include thyroid dysfunction with or without goitre, intellectual impairments, growth retardation, cretinism, increased pregnancy loss, and infant mortality. It is one of the most common causes of preventable impaired cognitive development [1,2]. According to results of a meta-analysis [3], children living in areas with iodine deficiency had intelligence quotient (IQ) 6.5-12.45 points lower than the IQ of those living in iodine-sufficient areas. Serious health consequences, such as cretinism and impaired brain development can be the manifestations of severe iodine deficiency [1][2][3]. Even mild iodine deficiency in pregnancy may lead to poorer cognitive outcomes in children, thus impairing their learning capacity and affecting the social and economic development of their countries [1,4]. These consequences of iodine deficiency are easily preventable by appropriate iodine intervention [1][2][3]5]. The World Health Organisation (WHO), the United Nations Children's Fund (UNICEF), and the International Council for the Control of Iodine Deficiency Disorders (ICCIDD) (now known as Iodine Global Network or IGN) have been assisting countries to implement appropriate strategies for the control and elimination of IDD worldwide [1,2,5]. Universal salt iodisation (USI), a policy of iodising all salt for human consumption, is the recommended strategy for the control and elimination of IDD in affected populations [1,2,5].
USI has been implemented in Papua New Guinea (PNG) since June 1995 following promulgation of the PNG Salt Legislation, banning the importation and sale of non-iodised salt [6]. The requirement to iodise salt was incorporated in the PNG Food Sanitation Regulation that was issued in 2007 [7]. The effective implementation of USI requires systematic monitoring of the program [1].
The PNG National Nutrition Survey conducted in 2005 provided national data indicating that 92.5% of households with salt had adequately iodised salt and that the iodine status among non-pregnant women of child-bearing age was adequate (170 μg/L) [8]. The report further indicated that 38% of households had no salt on the day of data collection, and women in these households had lower iodine status than those in households with salt (114 μg/L and 203 μg/L respectively). In contrast to these national figures indicating adequate iodine status, a number of mini-surveys on iodine status among children and non-pregnant women carried out from 1998 to 2016 indicated prevalence of mild to moderate iodine deficiency in some districts in PNG, such as in school age children in Hella district, Southern Highland province; pregnant and lactating women and infants 0-4 months in National Capital district; school age children in Aseki-Menyamya district, Morobe province and Lufa district, Eastern Highlands province [9][10][11][12][13]. Some of these areas are in remote mountainous regions, which may be more at risk of developing sub-optimal status of iodine nutrition [1][2][3]5].
A recent study in the remote and mountainous area in Kotidanga Rural Local Level Government (LLG) in Kerema district Gulf province in PNG reported moderate iodine status (median UIC 32.0 μg/L), stunting (57.6%), wasting (12.2%) and underweight (48.5%) among school children 6 to 12 years [14]. The authors indicated that more detailed study was urgently required to better understand the causes of the iodine status. The purpose of the current study was therefore to assess in more detail the iodine status and the knowledge, attitudes and practice (KAP) relating to the use of iodised salt in this remote community. This was done by determination of the discretionary per capita intake of salt per day, the availability of adequately iodised salt in households, the iodine status of school children (age 6-12 years) and the use of questionnaires to assess the KAP relating to the use of iodised salt.

Study site and population
The study site was Kotidanga Rural LLG area, in Kerema district, Gulf province, PNG. Gulf province has rugged mountainous terrains, grassland flood plains and lowland river deltas. It shares land borders with six other provinces: Central, Western, Morobe, Simbu, Southern Highlands and Eastern Highlands [15]. There are two districts in Gulf province: Kerema and Kikori. The capital of Gulf province is Kerema, which is located in Kerema district. Kotidanga Rural LLG is also located in Kerema district. The local population is mainly the 'Kamea', which are members of the Angan-speaking tribal group [15]. The population of Kotidanga Rural LLG is 45,385 [16]. In Kotidanga Rural LLG, there is one hospital at Kanabea village, established by the Catholic mission in 1964; one Health Extension officer is servicing a population of around 20,000 Kamea people [16,17]. Kotidanga Rural LLG is between 1200-1600 meters above sea level with temperatures between 12˚C and 30˚C and a yearly rainfall of 4000-7000 mm [18,19]. There are no roads to the study site; the only way of getting there is by walking along mountain paths or by air transport. It usually takes about 3 days walking during daylight from the location of the hospital to the closest settlement in Kerema, Gulf province or Menyamya, Morobe province. [20] a sample size of 300 school children was targeted for this study. Recognizing that typical samples size calculations cannot be undertaken for median UICs the UNICEF Guidance notes "Research indicates that around 400 urine samples per population group are required to measure the median UIC with 5% precision and 100 urine samples to measure the median UIC with 10% precision." Thus a sample size of 300 was considered to be adequate to provide sufficient precision in this small-scale survey with limited resources.

Study design and sampling
This was a prospective school and community based cross-sectional study carried out in Kotidanga Rural LLG in May-June 2017. There are 18 elementary, literacy and primary schools in Kotidanga Rural LLG. Simple random sampling was used to select nine literacy and primary schools in the study area. The total enrolments for each of the randomly selected schools, including the ages of children in each of the grades, were listed. According to school registers, the total number of eligible children in the age group 6 to 12 years was 632 children. A total of 32 (5.1%) children were absent on the day of urine collection. Multistage cluster sampling was used to randomly select 300 school children in the age group 6 to 12 years. A total of 289 (96.3%) children consented to participate in the study. For eleven (3.7%) children (7 girls and 4 boys), the parents and/or caregivers refused to give consent and/or children themselves refused to participate in the study.

Collection of samples
The objectives of the study were explained to the head of each school and to the teachers, who were requested to communicate the information to the parents or caregivers. The data collectors visited the households of children. A teaspoon of salt was collected from households with salt at the time of the visit. Three brands of commercial salt were found to be available in the markets. A sample of brand A, lot number 1, in a clear high-density polyethylene package of 250 g, was purchased at the market in Kotidanga (GPS coordinates: -7.386722, 146.003611). A sample of brand B, lot number 2, in a clear high-density polyethylene package of 250 g, was purchased at the market in Manimango (GPS coordinates: -7.309089, 145.919444). A sample of brand C, lot number 3, in a clear high-density polyethylene package of 250 g, was purchased at the market in Ipayu (GPS coordinates: -7.318624, 145.944936). These three samples were analysed for iodine content.

Discretionary intake of salt
To determine the discretionary intake of salt, sealed packets containing 250 g of iodised table salt were distributed to 30 randomly selected households of the 289 children. The number of individuals living in each household and eating food from the same cooking pot/hearth was counted and recorded. The head of the household was requested to use the salt as usual for cooking and eating. Each household was visited three days later to determine the amount of salt remaining in the packet. The number of individuals living in each household was again counted and recorded. The data obtained was used to estimate the average discretionary intake of salt per capita per day.

Urinary iodine concentration (UIC)
For the determination of UIC, single urine samples were collected at the school from each of the 289 selected school children, after obtaining informed consent from their parents or caregivers. Each urine sample was kept in a properly labelled sterile plastic tube with a tight-fitting stopper that was further sealed with special plastic band.

Questionnaires knowledge, attitudes and practices (KAP) regarding use of iodised salt
The semi-structured Food and Agriculture Organisation (FAO) of the United Nations nutrition-related iodine deficiency questionnaire [21] was adapted for use in this study. It was pretested in Kotidanga Rural LLG with 20 women 15-45 years old, recruited from five different villages in the district. Feedback and suggested changes were provided orally and in writing. This feedback was used to adapt and improve the questionnaire. It was then used to assess the KAP of randomly selected women visiting five markets from across the district, market stallholders selling salt, and important stakeholders (community leaders, teachers, health staff) in Kotidanga Rural LLG. Three women who were visiting markets refused to participate in the study.
The salt samples, urine samples and questionnaires were transported by airfreight to the Micronutrient Research Laboratory (MNRL) in the School of Medicine and Health Sciences (SMHS) University of Papua New Guinea (UPNG) for analysis.

Analysis of salt and urine samples
The WYD Iodine Checker [22] was used for the quantitative assay of iodine content in salt collected from the households and purchased in the markets. Salt samples from the market were assayed six times and samples from households two to three times each, depending on the amount of salt collected. The Westgard Rules using Levy-Jennings Charts were used for internal bench quality control (QC) for daily routine monitoring of performance characteristics of the WYD Iodine Checker. The percent coefficient of variation (CV) ranges from 2.5% to 5.0% throughout the analysis.
The UIC was determined by Sandell-Kolthoff reaction after digesting the urine with ammonium persulfate in a water-bath at 100˚C [1]. The Levy-Jennings Charts and the Westgard Rules were used for internal bench QC characterization of the assay method. The sensitivity (10.0-12.5 μg/L) and percentage recovery (95.0 ± 10.0%) of the urinary iodine (UI) assay were frequently used to assess the performance characteristics of the assay method. External QC monitoring of the assay procedure was by Ensuring the Quality of Urinary Iodine Procedures (EQUIP), which is the External Quality Assurance Program (QAP) of the Centers for Disease Control and Prevention (CDC), Atlanta, Georgia, USA.

Data analysis and interpretation
The Statistical Package for Social Sciences (SPSS) software (version 17) and the Microsoft Excel Data Pack 2010 were used for statistical analyses of the data. Shapiro-Wilks test was used to assess normality of the data. Mann Whitney U and Wilcoxon W tests were used for differences between two groups; Kruskal-Wallis and Friedman were used for comparison of all groups. A p-value of < 0.05 was considered as statistically significant.
The criteria used for interpretation of the salt iodine data were based on the PNG salt legislation [6,7]. According to the legislation all salt must be iodised with potassium iodate; the amount of iodine in table salt should be 40.0 to 70.0 ppm (mg/kg); the amount of iodine in other salt should be 30.0 to 50.0 ppm. These levels of iodine should be present at production or import level. WHO recommendations for iodine levels of food grade salt aim to provide 150 μg iodine per day, assume 92% bioavailability, 30% losses from production to household level before consumption and variability of ±10% during iodisation procedures [5]. If 30% of iodine is lost from salt iodised per PNG food regulations, iodine content of table salt at household level should be at least 28 ppm (40 ppm minus 30%). This implies that in PNG the iodine content in salt in retail outlets or at the time of consumption should be at least 28.0 ppm [6,7]. A cut-off of 30.0 ppm has been used in the analysis of this study by rounding up this figure. Global norms for iodine levels of salt at household level are 15 ppm based on the assumption that average salt consumption of 10 g per day would provide the adult iodine requirement of 150 μg per day [1]. Salt with iodine levels of less than 5 ppm is considered non-iodised salt [20]. For the UIC data, the recommended WHO/UNICEF/ICCIDD [1] criteria were used to characterise the status of iodine nutrition among the school children. According to the criteria, a population of school-age children is considered iodine deficient if the median UIC is below 100.0 μg/L. In addition, less than 20% of the urine samples should have UIC below 50.0 μg/L. The median UIC can also be used to indicate the severity of iodine deficiency; for example a population with median UIC < 20.0 μg/L is considered severely deficient; moderately or mildly deficient if it is 20.0 to 49.0 μg/L or 50.0 to 99.0 μg/L respectively [1].

Ethical approval
Ethical approval was obtained from the PNG National Department of Health Medical Research Advisory Committee (NDoH MRAC) and the Ethics and Research Grant committee in School of Medicine and Health Sciences (SMHS), University of Papua New Guinea (UPNG). Since the majority of the community cannot read or write, informed verbal consent was obtained from village authorities. Furthermore, each adult participant and primary caretaker of the children provided informed verbal consent. Participant consent was documented on each participant interview form. The ethics committees approved this consent procedure.

Availability of salt in households
Out of 300 school children selected, a total a total of 289 children agreed to participate in this study, which gave a response rate of 96.3%. Salt was available in 186 out of 289 households of participating children (64.4%). Salt samples were collected from all 186 households and analysed for iodine content.

Iodine content in salt from households and the markets
The mean (± STD) iodine content in salt from the households was 29.0 ± 19.1 ppm (mg/kg), the range was 1.3 to 58.2 ppm and the median was 30.5 ppm. The iodine content was below 30.0 ppm in 54.8% (102/186) of the salt samples, 31.2% (58/186) had iodine content below 15.0 ppm and 6.5% (12/186) had iodine content below 5.0 ppm.
Three brands of commercial salt were sold in the markets. One sample of each brand was purchased and coded as brand A, brand B and brand C. The mean iodine content in brand A was 35.6 ± 6.0 ppm and median was 32.5 ppm. For brand B the mean was 40.0 ± 0.8 ppm and median was 36.5 ppm. In brand C, the mean was 46.9 ± 2.0 ppm and median was 43.6 ppm. Thus, the iodine content of samples of all three brands collected in the market was above 30.0 ppm as would be expected based on required iodine content at production/import level indicated in the PNG Food Sanitation Regulations for commercial salt [7].

Discretionary per capita intake of salt and estimated per capita intake of iodine
The mean per capita discretionary intake of salt was 2.9 ± 1.8 g/day, with a range of 1.1 to 7.6 g/day and median of 2.3 g/day. The mean iodine content in the salt from the households was 29.0 ± 19.1 ppm. Thus, with a mean discretionary intake of 2.9 g of salt per capita per day, the calculated mean discretionary intake of iodine per capita per day was 84.1 ± 34.6 μg. Assuming that 20% of the iodine in salt is lost during storage and food preparation [1], the calculated per capita discretionary intake of iodine becomes 67.3 μg per day. This is below the 90.0 μg to 120.0 μg recommended daily requirement of iodine for school age children and 150 μg requirement for adults [1].

Urinary iodine concentration (UIC)
A single urine sample was collected from each of the 289 school children. The Shapiro-Wilks test for normality indicated that the frequency distribution curve of the UIC (μg/L) for all the children was not normally distributed (p = 0.001). The summary statistics of the UIC for the 289 children are presented in Table 1. The median UIC was 25.5 μg/L and the Interquartile Range (IQR) was 15.0 to 47.5 μg/L. In addition, 76.5% (221/289) of the children had UIC below 50.0 μg/L. The median UIC of 25.5 μg/L indicates moderate iodine deficiency. It is notable that this is not far from <20.0 μg/L, which is the cut-off point for severe iodine deficiency.  The UIC data for all 289 children were divided according to gender for further statistical analysis. Thus, of the 289 children, 175 (60.6%) were males and 114 (39.4%) were females. The median UIC for the male children was 25.0 μg/L and for the female children was 29.5 μg/L. Using the Mann-Whitney U and Wilcoxon W tests, no statistically significant difference (p = 0.264, 2-tailed) was indicated between the UIC of the male and female children. This was further confirmed by the Kruskal Wallis and Chi-Square tests (p = 0.254, 2-tailed). The UIC was below 50.0 μg/L in 80.0% (140/175) of male children and 69.3% (79/114) of the female children. The median UIC for both the male and female children indicated moderate iodine deficiency.

Comparison of the UIC of children from households with and without salt
The 289 UIC results were also divided based on the availability of salt in the households of the children on the day of the visit. Of the 289 households salt was collected in 186 (64.4%), but not available in 103 (35.6%) of the households.
The summary statistics of the UIC data for both cases are presented in Table 1. The median UIC was 34.3 μg/L for children in households with salt, indicating moderate iodine deficiency; compared to 15.5 μg/L for children in households without salt, indicating severe iodine deficiency. Statistically significant difference (p = 0.02; 2-tailed) was indicated between the UIC of children in households with salt compared to those in households without salt. The UIC was below 50.0 μg/L in 72.0% (134/186) of children in households with salt compared to 82.5% (85/103) of children in households without salt.
Although no detailed physical examination of the children was carried out, they were briefly seen by a general practitioner with experience in child health in low resource settings. No visible goitre was identified in any of the children.

Assessment of knowledge, attitudes and practices (KAP)
All five markets across the study area were visited. Women visiting the markets to purchase items and stallholders selling salt in the markets were randomly selected to participate in this section of the study. In addition, important community stakeholders in their place of work (community leaders, teachers, and health staff) were also selected. The variation in the number of participants in the three groups was due to logistical reasons.

Women visiting markets
A total of 153 women completed the questionnaires. The mean age of the women was 32.3 ± 8.2 years, the range was 18.0 to 50.0 years and the median age was 32.0 years.
The questionnaire results are presented in Table 2. The results show that 91% of the women cannot read, 87% do not listen to radio and 97% indicated that they do not work for money. In response to questions on the use of salt, 47% reported to always use salt at home, 49% reported they do not always use salt at home and only buy salt when they have money and 4% reported to use only traditional salt. Of the 47% that always use salt at home, 57% reported they use salt for cooking only and 43% use it for cooking and also adding to food before eating. When asked about iodised salt, 15.5% indicated to have some knowledge and 84.5% did not have any knowledge about iodised salt. Furthermore, 65% of the women reported they store salt in a bamboo stem covered with a leaf and 35% store salt in the original plastic bag. A total of 86% said it is good to prepare food with salt, 14% were unsure about salt in food; 88% indicated that it is difficult to buy salt because they usually do not have money and 5% indicated salt is not available.  How good do you think it is to prepare meals with iodised salt?

Stallholders selling salt
Gender distribution of the 36 stallholders selling salt that participated showed 23 (64%) were male and 13 (36%) were female. The combined mean age was 30.4 ± 5.6 years, the range was 22 to 45 years and the median age was 30.0 years. The questionnaire results are presented in Table 3. Among the stallholders 67% reported that they cannot read and 67% do not listen to

Stakeholders in the community
A total of 43 important stakeholders (community leaders, teachers, and health staff) from 9 villages across Kotidanga Rural LLG participated in this component of the study. When divided according to gender, 33 (77%) were males and 10 (23%) were females. Their combined mean age was 35.8 ± 6.4 years, the range was 26 to 57 years and the median age was 36.0 years. Table 4 shows the results from the questionnaires. All the stakeholders (100%) reported that they can read. Majority (74%) reported that they do not listen to the radio. Only 14% had knowledge about the use of iodised salt; 5% indicated that it is best to store iodised salt in a closed container at home; all of them (100%) indicated that people do not buy salt because of lack of money to purchase it. Furthermore, 92% responded that they do not have any knowledge about iodine deficiency; 89% do not know how iodine deficiency could be prevented, but 11% stated that they were using iodised salt and 72% indicated that it is good to prepare food with iodised salt. All (100%) indicated that it is difficult for community members to purchase salt mainly because they do not have money.

Discussion
According to recent WHO guidelines, all food-grade salt, used in household and food processing, should be fortified with iodine as a safe and effective strategy for the prevention and control of IDD in populations living in stable and emergency settings [5]. Salt is considered an appropriate vehicle for fortification with iodine because it is widely consumed by virtually all population groups in all countries with little seasonal variation in consumption patterns [5]. Thus, a basic premise of the WHO-recommended strategy is that all or, at least, the majority of households would have salt. In addition, at least 90% of households in a representative population should have salt with iodine content between 15.0 and 40.0 ppm [1]. In this study, salt was not available in 35.6% of the households on the day of the visit, contrary to the basic premise of the WHO recommendation. Most likely, it was not in the household because it is considered not affordable and only limited amounts are occasionally purchased. This finding is similar to that of the PNG National Nutrition Survey of 2005, which recorded that 38.0% of households sampled for this survey had no salt on the day of data collection; this proportion was as high as 50.0% in the Southern region and between 32.0% and 36.0% in the remaining regions; it was 42.0% in the rural areas [8]. Kerema district, the site of the present survey, is in Gulf province, which is in the Southern region.
In the present study 45.2% of the 186 households with salt on the day of the visit had adequately iodised salt according to the PNG Salt legislation This result was lower than those in other studies in various districts in PNG that reported higher percentage of households with adequately iodised salt; 95.0% in Hella District in 2004 [9], 94.5% in National Capital district in 2006 [23], 95.0% in National Capital district in 2009 [11], 78.0% in Morobe and Eastern Q9 What could be the consequences or health risks for the unborn baby of a lack of iodine in the diet of a pregnant woman?
(1) Risk of being mentally impaired 6 (3) (2) Risk of being physically damaged 2 (1) Highlands Provinces in 2013 [12]; and 66% in Karimui-Nomane district. However, the result was higher compared to 28% in Sina Sina Yonggomugl district, Simbu Province in 2017 [24]. Using the WHO/IGN/UNICEF global cut-off for adequately iodised salt at household level (� 15.0 ppm), 68.8% of the 186 households had salt with sufficient iodine content [1]. This is significantly lower than the WHO/IGN/UNICEF recommended 90% coverage that should indicate effective implementation of the Universal Salt Iodisation strategy [1].
This study found that the mean and median iodine content of salt in the households were lower than the salt samples collected in the markets. Recognising that 92% of stallholders sold brand A (mean iodine content = 35.6 ppm), 6% sold brand B (mean = 40.8 ppm) and 2% sold brand C (mean = 46.9 ppm) a weighted average content of all salt at market level is 36.1 ppm compared to that at household level of 29.0 ppm. This suggests some losses of iodine between the market and households. Losses of iodine may occur because some stallholders repacked salt from the 250 g original packages into smaller amounts, in plastic bags or wrapped in paper or leaves or because most households (65%) reported storing salt uncovered in the home, close to the fire. These practices may result in significant loss of iodine as reported by several authors [25][26][27][28][29][30]. According to these authors, the loss of iodine in salt can occur under various conditions including the type of retail packaging using unconventional packets, storage and transport at temperatures above 30˚C and the high relative humidity. Furthermore, some iodine may be lost during preparation and cooking of meals; more than half of the women (57%) reported adding salt to water for cooking only to then discard the liquid bearing much of the salt.
A further limitation regarding the impact of salt iodisation in PNG is the apparent low consumption of discretionary salt identified in this study, with a mean daily per capita discretionary salt intake of 2.9 ± 1.8 g. In 2010, a systematic analysis of 24-hour urine sodium excretion and dietary surveys worldwide estimated the total salt consumption, including non-discretionary sources of salt. The study found salt intake to vary widely between countries-from 3.76 g/ day in Kenya to 14.3 g/day in Uzbekistan with a global average of 10.6 g/day [31]. The finding of this study was well below the lowest intake indicated in the systematic analysis [31] and the 6.23 g/day estimated for PNG [31]. The present study assessed the discretionary salt intake, which did not include, for example, salt contained in processed foods such as bouillon cubes or instant noodles, although these are not commonly used for food preparation in this community. Our current result was also lower than the values obtained in other studies in PNG that also assessed discretionary salt intake by the same method; 6.6 g in Lae city [13], 4.7 g in Morobe [12] and 5.0 g in Simbu province [24]. It was also below the 10.0 g per capita per day salt intake used in formulating the PNG standards for iodine content in salt indicated in the PNG Salt Legislation [6,7].
The identified low per capita discretionary intake of salt combined with the low iodine content in the salt from a proportion of the households resulted in the calculated low iodine (67.28 μg per day) per capita intake of iodine obtained in households with salt. This can lead to iodine deficiency among vulnerable groups in the community and is further exacerbated by the low access to commercial iodised salt recorded in this study.
In the present study the median UIC of all the children was 25.5 μg/L, indicating moderate iodine deficiency. A previous survey conducted in the same area in 2015, recorded a median UIC of 32 μg/L in school children [14]. Comparison of the current findings with those of 2015 suggests a further deterioration in iodine status among this vulnerable population group. No data on access to adequately iodised salt was collected in the 2015 study; only data on use of commercial salt was reported [14].
The present study found a statistically significant difference in the median UIC among children in households with salt (34.3 μg/L) and those in households without salt (15.5 μg/L), as well as a significant difference in the iodine levels of salt in households and from markets. The results indicate that the poor iodine status among the children is likely related to low access to commercial salt, low discretionary salt intake and inadequate iodine levels in a proportion of the limited amount of salt being consumed. Similar situations have been recorded in some other rural and remote communities in PNG, in Hella district, Southern Highland province; in Aseki-Menyamya district, Morobe province and Lufa district, Eastern Highlands province, Karimui-Nomane and Sina-Sina Yonggomugl districts in Simbu province [9,11,24]. While nationally iodine status may be adequate due to access to adequately iodised salt [8], there appear to be pockets of remote communities that have low access to commercial salt and are at risk of iodine deficiency.
The results of the KAP indicated that majority of the respondents in the three groups had very limited knowledge about the importance and benefits of using iodised salt and also the consequences of iodine deficiency on the health of the population. The regular diet in this remote community living at high-altitude and with high precipitation is low in natural sources of iodine; they rarely consumed fish or other sea-foods, thus risk of iodine deficiency is high without interventions to increase iodine intake [1]. Access to commercial salt was found to be very low in this community due to insufficient disposable income and remoteness, which drives up the cost of external commodities, such as salt. Poor re-packing and household storage and food preparation practices may also have caused losses of iodine from the small amount of salt consumed.
It is important to acknowledge the questionnaire used may have limitations. This questionnaire was based on a modified FAO questionnaire validated for use in developing countries [21]. Responses on the questions "do you use salt at home" and "do you use traditional salt" and "reasons why people are not buying iodised salt" may not reflect all the response options or are mutually exclusive.
Recognising that lack of access to commercial iodised salt is a major limiting factor in the effectiveness of salt iodisation in this community, interventions are needed to increase its availability, such as by subsidising transport costs, improving distribution networks or making it available in smaller, more affordable pack sizes. Alternative or complementary strategies to increase iodine intake should also be explored such as the fortification of alternative processed food vehicles that are more readily available, such as cereal grains including rice or wheat flour, edible vegetable oil, or condiments and seasonings [32], or targeted distribution of iodine or combined micro-nutrient supplements to vulnerable groups in the community, in particular women of reproductive age [33].
In addition, advocacy and health education to improve "health literacy" on the importance of consumption of iodised salt should be carried out among key target groups in the community [34]. These interventions should be aimed at improving demand for iodized salt and changing re-packing, storage and cooking practices in order to preserve the amount of iodine in the salt consumed. Any education, promotion and communication programs should be tailored to the low literacy levels of this community. Social mobilisers should carry out regular visits to the households for face-face discussion regarding the use of iodised salt, using appropriate visual resources and tools. The importance of iodised salt should be included in health education of children in schools, and in discussions in churches and markets. Similar approaches have been carried out in remote communities in other countries with reasonable success [28,[35][36][37][38].

Conclusions
In this remote community there is insufficient consumption of adequately iodised salt, as a consequence of (i) low access to and consumption of commercial salt due to cost and availability, (ii) loss of iodine from iodised salt due to re-packing and storage practices and (iii) low awareness of the importance of using iodised salt. There is mild iodine deficiency among school children in the 6 to 12 years age group in households with salt and severe deficiency in those households that did not have salt. A specially designed multi-intervention strategy to increase availability of commercial iodised salt and awareness of its importance is recommended to address these fundamental problems. Also other opportunities for increasing iodine intake need to be explored. Commitments at all levels of government are essential for successful implementation of such a strategy. Codling.