Iodine status and availability of iodized salt: An across-country analysis

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1 Iodine status and availability of iodized salt: An across-country analysis Sue Horton and Alexander Miloff Abstract Background. Iodine deficiency has serious consequences, and the Universal Salt Iodization initiative has attempted to reduce the extent of deficiency. Objective. We aim to see how far across-country variations in urinary iodine in school-age children can be explained by environmental factors, particularly soil iodine and the availability of iodized salt. Methods. We use simple multivariate regression for two separate datasets, one for 30 developing, and one for 13 developed, using data on availability of iodized salt and soil iodine levels. Results. Median urinary iodine excretion is significantly and positively related to household availability of iodized salt (elasticity, 0.73) for developing, but the soil coefficient is not significant, probably because the dummy variable is not well measured. For the developed, there is a positive and significant effect of salt penetration rates (elasticity, 0.83) and a positive and significant effect of soil iodine (elasticity, 0.77). There is also a suggestion that with more serious soil deficits are more likely to iodize salt, so that univariate regressions of urinary iodine excretion on salt availability or penetration rates underestimate the beneficial effects of iodized salt availability on iodine nutrition. Conclusions. There are limitations to cross-sectional (ecologic) studies such as this, and the data are not perfect. Nevertheless, the results provide support for policies to iodize salt, given the widespread deficiency of iodine in diets worldwide. Sue Horton is affiliated with the University of Waterloo, Waterloo, Ontario, Canada; Alexander Miloff is affiliated with Harvest Plus, Ottawa, Ontario, Canada. Please direct queries to the corresponding author: Sue Horton, University of Waterloo, 200 University Avenue West, Waterloo, ON N2L 3G1, Canada; sehorton@uwaterloo.ca. Key words: Across-country analysis, iodine deficiency, regression analysis, salt iodization, soil iodine, urinary iodine excretion Although considerable progress has been made in improving iodine status worldwide, particularly with the progress in the Universal Salt Iodization initiative, 1.8 to 2 billion individuals worldwide still have insufficient iodine intake [1, 2]. Unlike the case for many other micronutrients, it is often in the industrialized (particularly those where iodization of salt is not required) that deficiencies exist in certain population groups and regions. In the past, goiter rates were used as a key indicator of iodine status and were also used to link status with functional outcomes. However, when iodine nutritional status is changing, for example due to public intervention, goiter rates are no longer a good measure, since they respond only with a lag, whereas urinary iodine excretion () responds immediately [3]. is also a more sensitive indicator of mild deficiency, which may not be associated with visible goiter but may nevertheless be associated with damage to the brain. We use data from international databases to examine the relationship between the median of schoolaged children and the household availability of iodized salt (HAIS) for developing, using a dummy variable to control for soil iodine deficiency. (Household availability of iodized salt is defined as the percentage of households in which iodized salt was available in the household when surveyed: it does not imply that all salt consumed by the household is iodized.) We are able to construct a good database (where the and HAIS data are for the same year) for 30. We also analyze the results from a sample of industrialized for which soil iodine data are available from a database collated by the British Geological Survey (described in Johnson et al. [4]). We were able to obtain data for schoolchildren matched within a 5-year period to salt penetration rates (proportion of 214 Food and Nutrition Bulletin, vol. 31, no , The United Nations University.

2 Iodine status and availability of iodized salt table salt produced that is iodized) for 13 industrialized for which soil iodine data were also available. The next sections discuss in turn our data and methods, results, and conclusions. Data and methods Several previous researchers have noted the positive correlation of with HAIS in developing [5, 6] *. Our work differs from the previous acrosscountry analyses of developing in that we constructed a consistent dataset for the developing world, retaining only and HAIS data from the same year (in those cases where it took more than 1 year to collect the data, we retained observations only where one of the years overlapped with the year of the HAIS data collection). The World Health Organization (WHO) database [7] (described in Andersson et al. [8]) contains several hundred observations for different regions, different age groups, and different iodine measures (mean, median, percentage below various cutoffs). Likewise, the UNICEF database on HAIS [9] contains over 600 observations for developing for different years. (Note that UNICEF describes the data as Household Consumption of Iodized Salt, although availability would be more accurate.) There were, however, only 30 for which matching data are available to form a consistent dataset (data were available for more than one matching year for a subset of five ). It is methodologically preferred to use matching years; urinary iodine levels respond rapidly to adjustments of iodine in the diet, and with the move toward Universal Salt Iodization, both and HAIS have been changing in developing. We use median for schoolchildren. Iodine deficiency in children has been correlated with poorer performance on intelligence tests, and in some circumstances interventions have improved scores on cognitive tests [10]. Although the most serious adverse effect of iodine deficiency is damage to the fetus (UNICEF [1], page 3), there were too few data in the WHO database on in pregnant women to use for this study. One recent study [11] was able to identify only six recent national surveys that contained national data on both pregnant women and schoolchildren. For these six, the correlation coefficient between median in pregnant women and that in schoolchildren was , and in three of the six, the median in pregnant women revealed a public health concern that was not evident in the data for * Gorstein J. Tracking progress toward the elimination of iodine deficiency disorders in Indonesia, visit January. UNICEF Indonesia, 2005 (mimeo); Untoro, J. Presentation to Board of Network for Sustained Elimination of Iodine Deficiency, 2006 (mimeo). 215 schoolchildren. Our work also differs from previous work in that we use a dummy variable for environmental iodine deficiency [12], which in turn is constructed from the prevalence of goiter prior to program interventions [13]. This is only a crude variable, since some have regions of deficiency as well as regions of adequacy, and the larger the country, the more likely the heterogeneity across subregions. However, since policy on salt iodization is national in scope, there are reasons to conduct the analysis at the national level. The developing-country data are all listed in appendix 1. The developing-country data were analyzed by conducting population-weighted multivariate regressions, with as the dependent variable, and three independent variables: HAIS, an environmental deficiency dummy, and time. Time was included to capture effects such as improvements in quality monitoring in salt iodization programs over time due to technological improvements and learning by doing. Only one observation was included per country so as not to have an unbalanced dataset: for those five where more than one observation was available, the most recent observation was the one that was used. There are some limitations to the data. Countries do not necessarily have the same minimum cutoff level for salt iodization (the minimum required for universal salt iodization is 15 ppm, but some use 20 ppm), and have also varied their levels of salt iodization over time. In China, for example, it is possible to track changes over time and see that in 1997 and 1999, as population coverage first approached the 90% goal, levels overshot what was desired, and iodization levels were then adjusted downward to achieve the desired level. We cannot control for this intraprogram variability. The variable used (HAIS) does not necessarily measure whether salt is iodized to the mandated level, but only that it is iodized. (Some report the more accurate titration data; others may simply report data obtained using the less accurate rapid test kits.) Another issue is the presence of goitrogens in the diet. Thilly et al. [14] noted in early work that populations could have similar levels of, implying similar iodine intake, but different levels of observed goiter (regions with high reliance on cassava had higher goiter levels, which could be due to lower absorption). This implies some limitations of as a measure of iodine utilization in the body, but again, this cannot readily be controlled for in the present analysis. In addition to the developing-country database, we also constructed a database for developed. The developed-country database contained data on median, salt penetration data (data on HAIS are not generally available for developed ), and data on soil iodine from a database constructed by the

3 216 S. Horton and A. Miloff British Geological Survey (median soil iodine data were used to correspond to median ). It was not possible to obtain a large enough sample with data on and salt penetration from the same year, so data were used within the same 5-year period. Typically, the salt penetration rates have not changed considerably in the industrialized covered, since policies have not changed over the particular period considered. There may be variations across as to whether salt used in the food industry is also iodized, but we do not have access to data on this. The developed-country database is given in appendix 2. Soil iodine data are not a perfect guide to iodine uptake in agricultural products grown in a region, since this depends on many factors, such as soil chemistry. Local water iodine levels are considered a better indicator; however, there are very few of these data available. The soil database contains almost 2,400 observations from 38 (although for 10 of these there are only one or two data points). Of the 28 with three or more data points, 8 are developing and were included in the previous database because they have data on HAIS rather than data on salt penetration, leaving data for 20 industrialized. For these, data on and salt penetration could be matched with the soil data for 13 (only one observation was used for each country). It is possible that some kind of agricultural-production-weighted soil iodine database would be preferable, but this was beyond what could be constructed with the data available. Consumption also does not rely only on local food, and food from other regions (or other ) will weaken the link between soil iodine and. Previous studies have explored the relationship between human iodine status and iodine in soil, water, or plants in individual [15 18] and the implications for health of adding iodine to irrigation water [19]. Iodized table salt in developed is likely to have a less consistent effect on. Even in with mandatory fortification of table salt (Canada for example), the legislation does not necessarily apply to salt used in food processing. As incomes rise with development, households consume more and more processed and restaurant foods and hence obtain less iodine from table salt, and this is compounded by health advisories advising households to curtail added salt. The United States and Switzerland, for example, have recently observed declines in, and Switzerland adjusted the mandated amount of iodine in salt upward in 1998 to partially compensate. For developed, there are frequently alternative sources of iodine in the diet. The use of iodofers in the dairy industry and iodine supplements for cattle feed in the winter has meant that milk has been a good source of iodine in several, although this was not originally the motivation. Coastal communities in many have high consumption of marine products, some of which (such as seaweed) have high iodine levels. A few not included in the database, such as Thailand, practice iodization of products other than salt. Results The model estimated (using population-weighted least squares) was as follows: = b 0 + b 1 salt indicator + b 2 soil indicator + b 3 time + error term For developing, the salt indicator was HAIS and the soil indicator was a dummy variable, deficient/ not; for developed the salt indicator was salt penetration and the soil indicator was median soil iodine from the British Geological Survey (BGS) database. The time variable was a linear trend starting in 1990 to allow for possible effects of universal salt iodization in developing. It was not anticipated to have a particular effect in the developed. For the developing, the results (table 1) show that is related significantly to salt iodine as measured by HAIS, with an elasticity of 0.73 (this means that a 1% increase in HAIS is associated with a 0.73% increase in ). There is also a positive and significant time trend, suggesting that has been improving over time (probably because of improvements in policy implementation). The soil deficiency dummy coefficient is not significant and has the wrong sign ( is higher in the with a dummy variable indicating soil deficiency). For the industrialized, there is also a positive and significant effect of salt iodine as measured by salt penetration rates, with an elasticity of There is also a positive and significant effect of soil iodine, with an elasticity of Discussion These are cross-sectional results (an ecologic analysis) and as such are suggestive of the impact of national policy regarding salt iodization, although this is a different type of evidence from that provided by randomized, controlled interventions. For developing, our results confirm similar results from previous studies; the main improvement is that we use a consistent database with and HAIS data for the same year. Our results for developed are new, and there have not been previous across-country studies attempting to control for soil iodine. One issue suggested by the data for the industrialized is that policies are not implemented independently of environmental conditions. For the industrialized, the correlation between the salt

4 Iodine status and availability of iodized salt 217 TABLE 1. Regression results and variable means and standard deviations, for urinary iodine excretion () a Variable Developing Salt iodine (0.390)** Soil iodine (18.378) Time (1.996)** Constant (32.237) Industrialized (0.513)** (8.881)* Mean (SD), developing (29.159) (0.471) 11.6 (3.460) (46.389) Dependent variable (67.749) Mean (SD), industrialized (36.049) (2.285) (74.437) F statistic 20.78** 13.86** Adjusted R Degrees of freedom 3,26 2,10 *p <.05, **p <.01 (one-tailed test). a. Columns 2 and 3 are coefficients (standard errors in parentheses); columns 4 and 5 are means (standard deviations in parentheses). Variables are given to three decimal places. coverage variable and the soil iodine variable (table 2) is negative, albeit not significant given the small sample size. It is possible that governments are more impelled to act when there are visible consequences of dietary iodine deficiency. Thus, the fact that several cantons in Switzerland had widespread visible goiter may have made that country more likely to adopt widespread nationwide salt iodization than some of the neighboring where the public health issue was less visible. The fact that salt iodization had been shown to be safe, effective, and cost-effective was a necessary precondition. In such circumstances, the end result is that iodine deficiency is currently worse, not in those with the most deficient environments, but in those TABLE 2. Simple correlation coefficients for variables Developing (n = 30) HAIS HAIS ** Soil iodine (dummy) Industrialized (n = 13) Salt penetration Salt penetration Soil iodine HAIS, household availability of iodized salt;, urinary iodine excretion with milder deficiencies in their soil and water. Countries such as China and Switzerland (where there were overt cases of cretinism) currently have higher status than, for example, Hungary prior to recent improvements in salt iodization, or Russia currently, despite the fact that median soil iodine in both China and Switzerland is lower than in Hungary or Russia. We cannot fully explore the hypothesis that the greatest remaining deficiencies are in with higher soil iodine. Some with higher soil iodine (the United Kingdom and Ireland) attach an even lower priority to iodine deficiency as a public health issue, so that surveillance data are not even available, although concerns have been raised about emerging problems (for example, among pregnant women in Ireland in the summer [20]). Since WHO now encourages all member to monitor the state of iodine nutrition every 3 years [21], it is possible that a more complete picture will emerge. Given these determinants of policy, simple correlation (between and salt penetration, or between and HAIS) in fact underestimates the relationship between the two variables, and multivariate regression such as that undertaken here using soil iodine is required. We acknowledge the data limitations inherent in our analysis. However, the availability of comparable data internationally is improving, which will assist future research. Increased data on among pregnant women (or greater knowledge of how this correlates with data for school-age children) seems to be an urgent research priority.

5 218 S. Horton and A. Miloff Acknowledgments The authors would like to thank Lucie Bohac of the Iodine Network for encouraging and facilitating this study, Chris Johnson of the British Geological Survey for providing access to the soil iodine database, and Xiaodong Cai of UNICEF and Lisa Rogers of WHO for assistance in obtaining additional information on survey dates for UNICEF s global database on HAIS and the WHO database. Thanks also to Justus de Jong, Cria Perrine, Dick Hanneman, Kevin Sullivan, Arnold Timmer, and Frits van der Haar for useful comments on previous drafts. Sue Horton would like to thank Wilfrid Laurier University, her employer at the time the original research was undertaken; similarly, Alex Miloff would like to thank the Iodine Network. No outside research funding was used to support this work. APPENDIX 1. Developing-country database a Country HAIS (%) Salt date (µg/l) Soil deficiency dummy (1 = yes) Afghanistan Armenia Bangladesh Bhutan Bosnia Belize Brazil Bulgaria Burundi Cape Verde China Gabon Gambia Guinea Haiti Indonesia Côte d Ivoire Jordan Macedonia Myanmar Mongolia Philippines Romania South Africa Sri Lanka Turkmenistan Uzbekistan Yemen Zimbabwe Peru HAIS, household availability of iodized salt;, urinary iodine excretion a. See text for data sources.

6 Iodine status and availability of iodized salt 219 APPENDIX 2. Developed-country database a Country Salt penetration (%) Salt date b (µg/l) date Median soil iodine (µg/g) Armenia Australia Austria Czech Republic Germany Hungary Latvia Netherlands New Zealand Russia Spain Switzerland USA , urinary iodine excretion a. See text for data sources, except salt penetration sources as follows: Armenia [9]; Australia [22]; Austria, Germany, Netherlands, Spain, Switzerland [23]; Czech Republic [24]; Hungary [25]; Latvia [26]; New Zealand [27]; Russia [28]; USA [29]. b. Note that exact date is not available for Czech Republic and Latvia. References 1. UNICEF. Sustainable elimination of iodine deficiency. New York: UNICEF, Zimmermann MB, Jooste PL, Pandav CS. Iodinedeficiency disorders. Lancet 2008;372: De Benoist B, McLean E, Andersson M, Rogers L. Iodine deficiency in 2007: global progress since Food Nutr Bull 2008;29: Johnson C, Fordyce F, Stewart A. What do you mean by iodine deficiency? A geochemical perspective. ICCIDD Newsletter, May Available at: org/media/idd%20newsletter/ /may2003. htm. Accessed 10 April Zhao J, van der Haar F. Progress in salt iodization and improved iodine nutrition in China, Food Nutr Bull 2004;25: Timmer A. Sustainable elimination of iodine deficiency: regional overview and implications for Ukraine. Presentation at Bioethics Conference, Ukraine, 1 October Available at: mp/02_01_2004_alm1.ppt. Accessed 10 April WHO Global Database on Iodine Deficiency. Available at: Accessed 10 April Andersson M, Takkouche B, Egli I, Allen HE, de Benoist B. Current global iodine status and progress over the last decade towards the elimination of iodine deficiency. Bull World Health Organ 2005;83: UNICEF Global Database on Iodized Salt Consumption. Available at: Accessed 10 April Zimmermann MB, Connolly K, Bozo M, Bridson J, Rohner F, Grimci L. Iodine supplementation improves cognition in iodine-deficient schoolchildren in Albania: a randomized, controlled, double-blind study. Am J Clin Nutr 2006;83: De Benoist B, McLean E, Andersson M, Rogers L. Iodine deficiency in 2007: global progress since Food Nutr Bull 2008;29: ACC/SCN (Administrative Committee on Co-ordination, Sub-Committee on Nutrition). First report on the world nutrition situation. Geneva: UN ACC/SCN, Kelly FC, Snedden WW. Prevalence and geographical distribution of endemic goiter. Bull World Health Organ 1958;18: Thilly CH, Swennen B, Moreno-Reyes R, Handlet JY, Bourdoux P, Vanderpas JB. Maternal, fetal and juvenile hypothyroidism, birth weight and infant mortality in the etiopathogenesis of the IDD spectra in Zaire and Malawi. In: Stanbury JB, ed. The damaged brain of iodine deficiency. New York: Cognizant Communications, 1994: Fordyce FM, Johnson CC, Navaratna URB, Appleton JD, Dissanayake CB. Selenium and iodine in soil, rice and drinking water in relation to endemic goiter in Sri Lanka. Sci Total Environ 2000;263(1-3) : Yang X-E, Chen W-R, Feng Y. Improving human micronutrient nutrition through biofortification in the soilplant system: China as a case study. Environ Geochem Health 2007;29: Gbadebo AM, Oyesanya TM. Assessment of iodine deficiency and goiter incidence in parts of Yewa area of Ogun state, southwestern Nigeria. Environ Geochem Health 2005;27: Abrahams PW. Soil, geography and human disease: a critical review of the importance of medical cartography. Progr Phys Geogr 2006;30:

7 220 S. Horton and A. Miloff 19. DeLong GR, Leslie PW, Wang S-H, Jiang X-M, Murdon AR, Jiang J-Y, Ma T, Cao X-Y. Effect on infant mortality of iodination of irrigation water in a severely iodinedeficient area of China. Lancet 1997;350: Nawoor Z, Burns R, Smith DF, Sheehan S, O Herlihy C, Smyth PP. Iodine intake in pregnancy in Ireland a cause for concern? Ir J Med Sci 2006;175: WHO Health Assembly resolutionwha Available at: WHA58/WHA58_24-en.pdf. Accessed 28 April Li M, Chapman S, Agho K, Eastman CJ. Can even minimal news coverage influence consumer health-related behavior? A case study of iodized salt sales, Australia. Health Educ Res 2008;23: European Salt Producers Association. Synopsis of regulations governing salt iodisation in EU Member States and penetration rate according to market segments. 24. Kusic Z. Iodine prophylaxis in Croatia: From severe endemic goiter to iodine sufficiency. ICCIDD Newsletter 2003;19(2). Available at: org/media/idd%20newsletter/ /may2003. htm. Accessed 27 April Kozma A, Gimesi A, Muzsnai A, Peter F. Urinary iodine excretion of Hungarian schoolchildren; Improvement during the last decade. Presented at Jubilee Meeting of the Hungarian Section for Pediatric Endocrinology (HSPE), Budapest, 27 April Abstract available at: Accessed 27 April Andersson M, de Benoist B, Darnton-Hill I, Delange F, eds. Iodine deficiency in Europe: a continuing public health problem. Geneva: World Health Organization/ UNICEF, UNICEF. The state of the world s children Table 2. Available at: tables.php. Accessed 10 April UNICEF. The elimination of iodine deficiency: A resource package for Central and Eastern Europe and the Confederation of Independent States: Russia Federation Fact Sheet, Available at: org/iodine/03_country/rus/03_17_rus.html Accessed 10 April Salt Institute. Iodized salt & other additives. Available at: Accessed 27 April 2010.