The evolution, progress, and future direction of Nepal's universal salt iodization program

Abstract Nepal is located in what was once known as the Himalayan Goitre Belt and once had one of the highest prevalence's of iodine deficiency disorders in the world. However, through a well‐executed universal salt iodization program implemented over the past 25 years, it has achieved optimal iodine intake for its population, effectively eliminating the adverse consequences of iodine deficiency disorders. A comprehensive review of policy and legislation, surveys, and program reports was undertaken to examine the key elements contributing to the success of this program. The paper reviews the origins and maturation of salt iodization in Nepal, as well as trends in the coverage of iodized salt, the iodine content in salt, and population iodine status over the past two decades. The paper describes critical components of the program including advocacy efforts, trade issues with India, the role of the Salt Trading Corporation, monitoring, and periodic program reviews. The paper discusses the recent findings from the 2016 national micronutrient survey demonstrating the success of the salt iodization program and describes emerging challenges facing the program in the future.


| INTRODUCTION
In 2016, Nepal conducted a nationally representative micronutrient status survey, which provided evidence of the remarkable progress that the country has made towards the reduction of vitamin A deficiency, anaemia, and improvement in iodine status (UNICEF, 2016). The survey provided updated estimates on the coverage and reach of large-scale interventions, including universal salt iodization (USI) as reflected by the proportion of households with access to adequately iodized salt (HHIS). These data indicate that Nepal has achieved optimal iodine intake through USI, thus reducing the risk of cognitive impairment among newborns born today and enabling children to thrive. This success is the result of a number of critical factors, including early recognition of the problem, political commitment, establishment of an exclusive agency responsible for the importation, storage and distribution of iodized salt from India (the Salt Trading Corporation [STC]), development of strategic plans of action that defined priority actions, early adoption of legislation that stipulated that all edible salt be iodized (USI), periodic surveys that tracked performance and implementation, and the deployment of targeted communications to encourage consumer demand to shift towards a higher quality product with adequate iodine levels. Furthermore, these elements are well established within the national nutrition architecture, which will contribute towards the sustainability of this success, including mandatory salt iodization, monitoring of imported salt, inclusion of iodine in the multisectoral nutrition strategy, and continuing to track iodine intake, as was done in the recent survey.
As with any success, future changes and revisions need to be anticipated. Consumer preferences can change. Salt reduction strategies may lead to an overall decrease in the intake of salt, whereas dietary patterns lead to an increased proportion of salt consumed in processed foods and condiments instead of on a discretionary basis. Although there is currently no monitoring system tracking salt consumption patterns, this will become increasingly important to determine whether to adjust the iodine standards in iodized salt.
Political will may shift away from nutrition, and anti-regulatory forces may change the ability to ensure the exclusive import of iodized salt. Weakened monitoring systems may allow noniodized or inadequately iodized salt to enter Nepali markets. The purpose of this paper is to highlight the remarkable success Nepal has achieved and the key factors responsible, while discussing future directions for ensuring and sustaining optimum iodine nutrition in Nepal.

| METHODS
The paper is based on a comprehensive review of past and current surveys, research papers, legislation, trade documents, policy statements, and national strategic plans. The review focused on key program elements, including political commitment, partnership, monitoring systems, social mobilization, and trade issues. Trend analysis for key indicators is based on four nationally representative surveys conducted in 1998 (Government of Nepal, 1998), 2005(Government of Nepal, 2005, 2007 (Government of Nepal, 2007), and (Government of Nepal, 2016, which characterized and captured critical changes in USI program performance resulting from programmatic adjustments and refinements. In addition, a number of subnational surveys have also been reviewed and discussed. For review of salt iodine content, only reports and papers that have utilized titration method have been selected, and findings based on rapid test kit method have been excluded.
The findings will focus on historical context, salt iodization program implementation, monitoring salt iodization consistency, marketing to improve uptake, and trends in key indicators and impact on status.

| RESULTS
3.1 | The early years: Recognizing the problem of IDD and adopting the challenge of USI Iodine deficiency was recognized very early in South Asia, including Nepal. Perhaps as early as 200 BC, goitre was described in Indian medical texts, and Chinese sources suggest use of marine plants for its treatment as early as 100 BC. Reports from British visitors to Nepal in the late 1700's noted a high prevalence of goitre and cretinismattributed to a wide variety of causes by the local population. Work in India began to focus on iodine as a treatment, and in 1832, Joseph Bramley, the Medical In-Charge at the British Residency in Kathmandu, presented on use of iodine in the treatment of goitre. There were accounts of tens of thousands of cases of goitre treated in the Nepal Terai by British medical officers in the ensuing years (Miles, 1998).
The world began to recognize the importance of iodine deficiency and its global distribution in the mid 1980's, as research studies established links between suboptimal iodine and brain development, although a large number of surveys demonstrated significant iodine deficiency in many more countries than expected. (Delange, 2000;Hetzel & Pandav, 1996). With the World Summit for Children in 1990, iodine deficiency was established as a critical public health issue. This was followed by a declaration by the 43rd World Health Assembly, which stated that "WHO shall aim at eliminating iodine deficiency disorders as a major public health problem in all countries by the year 2000" (World Health Organization, 1990).
Nepal responded quickly to the challenge of elimination in response to early subnational surveys showing high goitre rates.
Although Nepal imported iodized salt from India as early as 1973 and initiated iodized oil supplementation in target districts in 1979, small surveys continued to show severe iodine deficiency, including one in 1980 that "found 107 cretins and/or deaf mutes in a population of 2,456 persons in the northernmost community (of Dolakha District) bordering Tibet" (Achard, 1987). The magnitude of the problem was even reported in the New York Times, commenting on the "Himalayan goiter belt," mentioning the injection program, and the early but ineffective salt iodization in India (Eckholm, 1985). Clearly, there was strong interest in the problem of goitre and cretinism both in Nepal and India, but early on, the challenges of addressing the problem at the national level seemed overwhelming. Experts suggested that "the

Key points
• Nepal has achieved adequate iodine intake through a successful salt iodization program.
• The recent micronutrient survey confirms this success, demonstrating high use of adequately iodized salt and adequate iodine intake all population groups sampled.
• The program success is based on ongoing advocacy, strong legislation mandating iodization, routine monitoring at border stations, consumer education through communication campaigns, and periodic program reviews.
• Future challenges include managing the iodine content in iodized salt to salt to address excessive iodine in salt, understanding use of iodized salt in processed foods, and insuring program visibility to ensure sustainability.
undoubted progress that has occurred in understanding goitre and cretinism, and knowledge of their treatment has yet to be universally applied. To do so is technically feasible in South Asia, though questions remain on epidemiology, and there are serious doubts whether the sociopolitical will exists to tackle the problem" (Miles, 1998). 3.2 | Establishing national programs: Addressing goitre and establishing importation of iodized salt "recognized Nepal's right to import and export commodities through Indian territory and ports." Given Nepal's geography, this treaty was critical for the supply of goods to the country. Diplomatic issues over the years have resulted in restrictions of this flow of goods from India, such as the closure of entry points by India in 1989, although this did not hinder salt availability due to a policy to have a 6-month buffer stock. (Nations Encyclopedia, 1991) Virtually, all salt consumed in Nepal comes from India, with some entering through China for some areas where road access to China is close. As early as 1963, the STC was established as a public-private partnership to manage import and distribution of salt. Although this early effort did establish a mechanism to import and distribute salt, little attention was given to the quality of iodization, either at the point of production in India or upon importation to Nepal.
The global attention on IDD and its elimination through USI intensified in the mid-1980s and recognizing the cost and logistical difficulties with the injection program, Nepal began to focus increasingly on ensuring that all salt imported from India was iodized. Salt iodization units were established at five key border entry points, which iodized inadequately iodized shipments. In addition, in the 1980s, the STC started packaging and marketing refined and crushed iodized salt in 1-kg consumer packages. The salt trade in Nepal has been regulated by several legislative acts. On the basis of the Export and Import (Control) Act, 2013Act, (1957

| Improving the consistency of iodization
Longstanding cultural preference in Nepal was for coarse, unrefined salt called "Phoda" salt-in 1998, less than 10% of the population used refined salt and nearly 65% of the Nepali population (80% of the hill population) used phoda salt with the balance consuming crushed salt.

| Shifting consumer preference to refined salt
The program matured and was equipped with evidence that salt was iodized, but the consumer-preferred phoda salt continued to be unlikely to meet standards. In response, the government focused on establishing ways to shift consumer preference to a more refined consumer packaged product that would stabilize the iodine content of salt. For many years, the coarser phoda salt continued to be the preferred salt, particularly in the mountains.
Although STC was the sole importer of edible salt, there was such a high demand for phoda salt, especially in the mountains, and it was not possible to simply discontinue the supply. However, as more processed refined salt was introduced and available more widely, consumers began to increase their purchase of a more refined, cleaner packaged salt that they did not need to wash There was a clear association between the iodine content and the type of salt used. Among refined salt samples, 97% contained >15 mg/kg, whereas the percentage of phoda salt with this level of iodine was only 46%. These data represent a dramatic progress for the salt iodization program, which has clearly resulted from a shift in consumer preference from coarse, phoda salt with inconsistent iodization, to the use of refined salt that is more consistently adequately iodized.
Refined salt has much greater retention of iodine than large crystal salt, and this feature has translated to a greater effectiveness of the salt iodization program (Figure 4). In 2016, there was a clear association between the iodine content in HHIS and the iodine status of the population (Figure 6).
The mUIC value in SAC from households with low iodine in HHIS salt (<15 mg/kg) was 162 ug/L and increased to 249 ug/L among SAC from households whose HHIS content was adequate (15-40 mg/kg). Finally, among those SAC whose HHIS content was high (>40 mg/kg), the mUIC was 419 ug/L. These patterns were seen in earlier surveys, but the most recent data lead to several observations. First, even among households with low iodine in HHIS, the iodine status was classified as optimal suggesting that there may be other sources of iodine in the diet than solely the iodine from household iodized salt. Second, the iodine status of SAC in households with high iodine content led to an excessive iodine intake, and although this is likely not to translate to significant pathology of adverse consequences, it does inform potential program adjustments, for example, decreasing the standard for the iodine content in refined iodized salt.

| DISCUSSION
The 2016 national micronutrient survey serves as a benchmark for progress to date, based on a number of program performance metrics. Clearly, efforts to increase the availability of iodized salt and improve iodine status have been successful. These achievements in the USI program are a direct reflection of the fact that the enabling environment has worked to improve consistency in iodization and use of iodized salt.
Nepal has in essence achieved optimal iodine nutrition, and its success should be celebrated. At the same time, it is important to understand key program elements that have led to the success and that can be strengthened in order to assure its sustainability. Many things likely contributed to this success: Factors contributing to success currently classified in the "excessive" range, whereas pregnant women and women of child bearing age would be classified as "adequate" and "more than adequate," respectively. Looking at the stratified results for several subgroups in the population, among the 34 strata listed, 19 (56%) were classified as excessive for SAC.
Iodine intake was high in the central and western regions, in the Terai, and among a number of ethnic groups including the poorer Terai Janajati. For pregnant women, there were no strata with mUIC >500, but again, the sample size was small rendering these estimates imprecise. In addition, the assessment of iodine content of salt showed that mean iodine content for all salt samples was 44.1 ppm, and that 67.5% were >40 ppm-well above the expected level at the retail (30 ppm) and household (15 ppm) levels. The standards are based on an average per capita consumption of 10-g salt per day, so an iodine content this high will provide more than three times the daily requirement.
These findings suggest that the current standard, combined with marked increase in use of a refined packaged product, may require an adjustment of the standard. The Nepal regulation/standard for iodized salt was developed when salt quality was poor, when packaging was suboptimal, and when losses of iodine were anticipated during transportation and storage. The shift toward a refined consumer packaged F I G U R E 6 Population iodine status-by iodine content in salt F I G U R E 5 Iodine content in HHIS-by ecological region product has likely limited losses, allowing the accepted production level (50 ppm) to persist to the household level.
The STC continues to be the sole salt trade agency responsible for importing and distributing iodized salt. Salt imported by parties other than STC through the porous international boarder is regarded as unregulated and illegal by law. This in theory helps limit the amount of poorly iodized salt entering the country.
The current Nepal standard differs from the standard in India.
This has resulted in most imported salt coming from larger sophistocated producers in India that meet the Nepal standard. Harmonizing the standard may result in a larger pool of producers supply Nepal's needs, potentially affecting the quality of iodization and increasing the amount of poorly iodized salt coming across the porous border.

| Dietary changes
Currently, the evidence from the 2016 survey suggests a good correlation between the iodine levels of salt consumed in households and iodine status. However, dietary patterns change, and with a movement toward increased consumption of processed foods (including packaged soups), the situation in Nepal will need to be monitored closely. It may be useful, for example, to consider an assessment of processed food consumption and, more specifically, the contribution of these foods to salt consumption. Because salt for human consumption is primarily provided through STC, it is likely that virtually all processed foods produced in Nepal use iodized salt. However, shifting patterns of household salt use and introduction of new products may make it important to understand this contribution.
The disease patterns in Nepal have also changed, with a growing problem with chronic diseases including diabetes, heart disease, and hypertension. (Mohan & Prabhakaran, 2013) With the global movement toward salt reduction, the multisector action plan for the prevention and control of non-communicable diseases (2014-2020) of the government of Nepal has target of 30% relative reduction in mean population intake of salt (Government of Nepal, WHO, 2014-2020). Whereas it is relatively easy to adjust the standards for iodized salt to accommodate these changes, it is considerably more difficult to understand how effective a salt reduction recommendation is in reducing salt intake. This will require careful review and monitoring of salt reduction strategy implementation in the country.

| Sustaining the enabling environment
The government of Nepal has been attentive to the issue of iodine deficiency for several decades and has included iodine program elements in the recent multisectoral nutrition strategy. In some countries, once certain benchmarks were reached, there was less interest in IDD, and in some instances, there was backsliding.
Seemingly innocuous changes, for example, in the wording of legislation, can result in weakening of the IDD program (Codling et al, 2017). Other priorities can limit funding for critical elements of the program. None of this has happened in Nepal, and the current survey again suggests that the micronutrient component of the nutrition of women and children remains a high priority despite gains made. This suggests that the basic foundation for a sustained enabling environment is well established. With a shift in focus to a broader approach to nutrition, and on reduction in stunting, it will be critical to ensure that the monitoring of micronutrient deficiency continues so the changes noted above do not adversely affect the sustained elimination of IDD.

| CONCLUSION
Nepal has effectively eliminated IDD as a public health problem through a successful USI program. The most recent survey confirms this success but suggests some consideration should be given to several program areas: • Review and consider reduction in the standard for production and retail salt iodine levels. This should be done in consultation with all relevant stakeholders to ensure that imported salt meets the new standard, and that inadequately iodized salt coming across the porous border does not increase.
• Ensure the adequacy of ongoing monitoring of imported salt to track any changes in sources and quality. Complement this with periodic assessments of iodine status • Consider a brief review of salt used in the processed food industry and the consumption of processed foods and condiments with a high salt content in Nepal-to anticipate the likely increasing trend and its implication for the USI program • Establish a review mechanism that triangulates data on salt consumption, iodine status, and sources of salt in the diet, which will allow for rapid change in the iodine standard for salt in the event of successful salt reduction strategies

ACKNOWLEDGMENTS
The authors would like to acknowledge the assistance for preparation of this article from the UNICEF nutrition team in Kathmandu, as well as other IGN members who helped with editorial review. The authors would like to thank Dr. CS Pandav for assisting with summarizing the main points of the article during the review meeting in Kathmandu in 2018.

CONTRIBUTIONS
NP and SC contributed to the article through provision of reference material, editorial support, and drafting of some policy sections of the main text. JG, CP, and MRM contributed to the main text, data review, and editing. RH contributed by drafting the initial text, editing, and data presentation. KP provided input on the paper from the government IDD control program perspective.