Environmental iodine and the link with iodine deficiency disorders
Early 19th and 20th century studies indicated that places with goitre had lower water or soil iodine concentrations than places without goitre. However, these studies have not been critically reviewed in the light of modern chemical analyses and understanding about environmental iodine.
While there are reports indicating an inverse relationship between soil or water iodine and goitre or iodine deficiency, not all studies have confirmed this. For example, a comparison of environmental iodine at sites lying within the historical UK goitre belt (Stocks 1928; Phillips et al 1983) and sites outwith the belt showed no statistical difference in soil, water and atmospheric deposition concentrations in different datasets collected over a 50 year period (Stewart et al 2003). Equally, there has been no systematic comparison between soil or water iodine concentrations and the levels of disease in the local inhabitants.
Furthermore, It is possible that while local variations in disease rates may reflect local changes in iodine supply, there are other, usually unmeasured, factors (such as soil type, iodine bioavailability, local goitrogens [factors other than iodine deficiency that contribute to the development of goitre and other iodine deficiency disorders] or deprivation) which are influencing the prevalence of iodine deficiency disorders in undetermined ways. There is no recognised environmental standard for iodine concentrations with regard to the production or protection of the iodine deficiency disorders.
Many recent health-based sources, journal articles and websites on iodine – including the Comprehensive Handbook on Iodine edited by Preedy, Burrow and Watson (2009); Zimmerman 2009; Zimmerman 2012; the Global Iodine Network page http://ign.org/p142002146.html – have statements, without citation, on environmental iodine which are based on outdated beliefs around iodine transformations and movements in the environment. In fact, some of the statements made in these sources are known to be deficient themselves, or even incorrect. For example:
Statement: Leaching from glaciations, flooding, and erosion has depleted surface soils of iodide:
Comment: Water (cold or hot) is a poor remover of iodine from soils. Erosion and glaciers remove soil, not just soil components. Normal soil iodine levels have never been defined, nor have sufficient levels for human or animal health: the concept of iodine depleted soils is comparative, not normative.
The question about glaciation as a cause of iodine deficiency goes back to Goldschmidt, the father of modern geochemistry. He proposed a test, never undertaken, assuming that there has not been enough time since the Quaternary glaciations for soil iodine to reach equilibrium. This question of time to equilibrium has been challenged in the geographical literature as well as the geochemical. Merke wrote that as a glacier thickened down-valley it would remove more soil: but any glacier removes all soil. There is no environmental evidence that erosion by water reduces iodine concentrations. Iodine is poorly leached by water from soils.
References:
Fuge & Johnson 1986; Goldschmidt 1954; Krupp & Aumann 1999; Merke 1967; Pennington & Lishman 1971; Schnell & Aumann 1999; Stewart et al 2003; Whitehead 1984
Statement: Iodide ions (I–) in seawater are oxidized to elemental iodine (I2), which volatilizes into the atmosphere, completing the cycle by being returned to the soil by rain.
Comment: Iodine transfer between seawater and air is complex and is important in near-surface ozone destruction, organic chemistry and probably cloud formation. While inorganic iodine emission is the largest single source of iodine to the atmosphere, release from the sea is more than just volatilisation of I2. An important role is played by HOI and organic iodine compounds contribute as well. Oceanic organic iodine precursors include CH3I, C2H5I, C3H7I, CH2ICl, CH2I2, CH2IBr. Rain adds iodine to soil (somewhat in contradiction to the previous statement about leaching), but dry deposition is also important.
References: Baker et al 2001; Saiz-Lopez et al 2012; Sherwen et al 2015; Whitehead 1984
Statement: Atmospheric iodine is lost to the stratosphere.
Comment: This does not make physical sense: what about gravity? Does iodine accumulate in the stratosphere or is it lost outward to space? Most atmospheric iodine is found in the troposphere (usually <10 km) with very little reaching the stratosphere (between 30 to 50 km altitude). This is due to the short life (high chemical reactivity) of atmospheric iodine compounds: the longest lived, CH3I, has an atmospheric residence time of about 7 days, while the shortest can be measured in seconds (I2 15s) or minutes (CH2I2 4m). Compare this to the long-lived organic fluorine compounds that stay in the stratosphere for years, allowing a build-up of concentration with resulting high-altitude destruction of ozone.
References: Tegtmeier et al 2013
Statement: Iodine cycling in many regions is slow and incomplete, leaving soils and drinking water iodine depleted
Comment: Iodine cycling in many regions has never been fully explored: e.g. investigations into soil/water do not fully account for atmospheric deposition or plant uptake of iodine compounds. Depletion supposes a sufficient level to start with; but the concept of depletion (and initial sufficiency) is an assumption, not a proven fact. There is no agreed definition of environmental deficiency.
The best data on water iodine and its relation to disease come from Denmark, but other areas are not consistent with this: are there unrecognised local determinants in Denmark? What is the relationship between water iodine and human disease?
Recent work in the Alps suggest a tripling of iodine in Alpine ice between 1950 and 1990. This is consistent with increased iodine emissions from the oceans driven by increasing anthropogenic NOx emissions. Furthermore, historical soil records indicate that iodine input to soil greatly outweighs loss to herbage. In fact, the increase in soil iodine over 105 years was broadly consistent with estimated additions from rainfall and dry deposition
References: Andersen et al 2008; Bowley et al 2017; Landis et al 2012; Legrand et al 2018; Stewart et al 2003
Statement: Crops grown in these depleted soils will be low in iodine. Humans and animals consuming food grown in these soils become iodine deficient.
Comment: The soil-crop transfer of iodine is complex and not well understood. The dietary chain of iodine from soil and air to plant and food and humans/animals has not been clearly delineated. The atmosphere can provide enough iodine to explain plant concentrations.
References: Bowley 2013; Whitehead 1984
Statement: Distance from sea leads to iodine deficiency.
Comment: Iodine deficiency disorders are found in coastal populations; not all inland areas suffer from the deficiency disorders. This concept of distance from the sea influencing human or animal deficiency is based on old models and understanding of iodine mobility and transformations. The marine influence on soils extends inland for about 100 km, but the same concentrations of soil iodine found deep inland can be found within that 100 km as well, suggesting some soils closer to the sea are ‘polluted’ by extra iodine.
References:Johnson et al 2003
There is reason to believe that global circulation patterns will distribute iodine across the continents. After the Fukushima point-source release of radio-iodine, 129I was found around the globe (Masson et al 2011). In Taiwan iodine arrived from Japan via two pathways at different altitudes: 1) transported in the planetary boundary layer (low altitudes) by the northeast monsoon wind directly toward Taiwan; 2) transported in the free troposphere (above the boundary layer but below 10 km altitude) by the prevailing westerly winds around the globe (Huh et al 2012).
In other words, it is not clear why some defined geographical areas lead to higher prevalence of the iodine deficiency disorders than others. Is it the local environment, the dietary habits of the community, a result of some aspect of poverty and deprivation, or what?
The literature has a number of tantalising references to goitrogens, co-factors that, probably in the face of some deficiency of iodine supplies, enhance the deficiency and increase the resulting prevalence of the deficiency disorders. These include organics (Brassica vegetables, onions, millet, rape, white clover, cassava), minerals containing known goitrogens [tourmaline (BF4-), graphite shists (SO3F-),molybenite (MoO-), lithium mica (Li)], coal-derived dihydroxyphenols, deprivation, protein-energy malnutrition, and plate tectonics (Langer & Greer 1977, Delange 1982, Gaitan et al 1986, Stewart 1990, Johnson et al 2003). Their role remains mysterious.
- The UK Iodine Group is actively involved in reviewing the environmental determinants of iodine deficiency.
In 1941, Beeson wrote, “There are probably more contradictory data relating to the effect of soils on the occurrence of goiter troubles than to the occurrence of any other nutritional disturbance” (Beeson 1941, p22). This remains true today!
Beware the anthropological fallacy: the attribution of the characteristics of a population to the environment (Stewart et al 2003).
Some questions:
- What is the proportion of biological/organic iodine in soils and air?
- What are the mechanisms & rates of distribution of iodine in the atmosphere?
- What is the relationship between soil iodine bioaccessibility and the iodine deficiency disorders?
- What does stream iodine represent?
- What are the sources, pathways, and quantity of iodine that enters into our diet?
- What is the role of goitrogens in the causation of iodine deficiency disorders?
- Which determinants of the iodine deficiency disorders are global, which local?
- Can we improve prevention?
References
Andersen S et al (2008). Naturally Occurring Iodine in Humic Substances in Drinking Water in Denmark Is Bioavailable and Determines Population Iodine Intake. The British Journal of Nutrition. 99(2): 319–25.
Baker AR, Tunnicliffe C, Jickells TD (2001). Iodine Speciation and Deposition Fluxes from the Marine Atmosphere. Journal of Geophysical Research: Atmospheres. 106(D22): 28743–49.
Beeson KC (1941). The Mineral Composition of Crops with Particular Reference to the Soils in Which They Were Grown: A Review and Compilation. U.S. Dept. of Agriculture, 1941.
Bowley HE (2013). Iodine Dynamics in the Terrestrial Environment. PhD thesis, University of Nottingham. http://etheses.nottingham.ac.uk/3241/.
Bowley HE, Mathers AW, Young SD, et al (2017). Historical Trends in Iodine and Selenium in Soil and Herbage at the Park Grass Experiment, Rothamsted Research, UK. Soil Use and Management 33 (2): 252–62.
Delange FB (1982). Nutritional factors involved in the goitrogenic action of cassava. Ottawa: International Development Research Centre, 1982.
Fuge R, Johnson CC (1986). The Geochemistry of Iodine – a Review. Environmental Geochemistry and Health. 8(2): 31–54.
Gaitan E, Cooksey RC, Lindsey RH (1986). Factors Other than Iodine Deficiency in Endemic Goitre: Goitrogens and Protein Calorie Malnutrition (PMC). In Factors Other than Iodine Deficiency in Endemic Goitre: Goitrogens and Protein Calorie Malnutrition (PMC). Washington DC: Pan American Health Organisation, 1986. pp 28–45.
Goldschmidt VM. Geochemistry. Edited by Alex Muir. Oxford: Clarendon Press, 1954.
Huh C-A, Hsu S-C, Lin C-Y (2012). Fukushima-Derived Fission Nuclides Monitored around Taiwan: Free Tropospheric versus Boundary Layer Transport. Earth and Planetary Science Letters. 319–20: 9–14.
Johnson CC, Fordyce FM, Stewart AG (2003). Environmental Controls in Iodine Deficiency Disorders-Project Summary Report. Commissioned Report No. CR_03_058N, DfID KAR R7411. Keyworth: British Geological Survey. http://nora.nerc.ac.uk/8355/1/CR03058N.pdf.
Krupp G, Aumann DC (1999). The Origin of Iodine in Soil: I. Iodine in Rainfall over Germany. Chemie Der Erde-Geochemistry. 59(1): 57–67.
Landis JD, et al. (2012). Surficial Redistribution of Fallout 131iodine in a Small Temperate Catchment. Proceedings of the National Academy of Sciences. 109(11): 4064-4069
Langer P, Greer MA (1977). Antithyroid Substances and Naturally Occurring Goitrogens. Basle: Karger, 1977.
Legrand M, McConnell JR, Preunkert S, et al (2018). Alpine Ice Evidence of a Three-Fold Increase in Atmospheric Iodine Deposition since 1950 in Europe Due to Increasing Oceanic Emissions. Proceedings of the National Academy of Sciences of the United States of America, November, 12136–41.
Masson O. et al. (2011). Tracking of Airborne Radionuclides from the Damaged Fukushima Dai-Ichi Nuclear Reactors by European Networks. Environmental Science & Technology. 45(18): 7670–77.
Merke F (1967). Weitere Belege Für Die Eiszeit Als Primordiale Ursache Des Endemischen Kropfes: Eiszeit Und Kropf Im Wallis [Further evidence of the Ice Age as a primordial cause of endemic goiter: Ice Age and goiter in Valais]. Schweiz Med Wochenschr. 97: 131–40.
Pennington W, Lishman TG (1971). Iodine in Lake Sediments in Northern England and Scotland. Biological Revues. Cambridge Philosophical Society 46: 279–313.
Phillips DIW, et al. (1983). Mortality from Thyrotoxicosis in England and Wales and Its Association with the Previous Prevalence of Endemic Goitre. Journal of Epidemiology and Community Health, 37: 305–9.
Preedy V, Burrow G, Watson R (eds.) (2009). Comprehensive Handbook of Iodine: Nutritional, Biochemical, Pathological and Therapeutic Aspects. Amsterdam: Academic Press.
Saiz-Lopez A, et al. (2012). Atmospheric Chemistry of Iodine. Chemical Reviews. 112(3): 1773–1804.
Sherwen T, et al. (2015). Iodine’s Impact on Tropospheric Oxidants: A Global Model Study in GEOS-Chem. Atmos. Chem. Phys. Discuss. 15(15): 20957–23.
Schnell D, Aumann DC (1999). The Origin of Iodine in Soil: II. Iodine in Soils of Germany. Chemie Der Erde-Geochemistry. 59(1): 69–76.
Stewart AG, et al. (2003). The Illusion of Environmental Iodine Deficiency. Environmental Geochemistry and Health 25(1): 165–70.
Stocks, Percy (1928). Goitre in the English School Child. Quarterly Journal of Medicine, 21: 223–75.
Tegtmeier et al. (2013). The Contribution of Oceanic Methyl Iodide to Stratospheric Iodine. Atmos. Chem. Phys. 13(23): 11869–86.
Whitehead DC (1984). The Distribution and Transformations of Iodine in the Environment. Environment International .10(4): 321–39.
Zimmermann MB (2009). Iodine Deficiency. Endocrine Reviews. 30(4): 376–498.
Zimmermann MB (2012). Iodine Deficiency and Endemic Cretinism, in Werner & Ingbar’s The Thyroid: A Fundamental and Clinical Text. Lewis E. Braverman and David Cooper (eds.) 10th edition. Alphen aan den Rijn: Lippincott Williams & Wilkins, pp217–42.
Text written by Dr Alex Stewart (December 2015)
Annotated abstract from
Stewart AG. Iodine in the plant: there’s more going on than is usually realised: a literature review. Society for Environmental Geochemistry & Health annual meeting, Brussels, July 2016.
The amount of iodine intercepted by vegetation decreases with increasing rainfall, depending on the combined influence of biomass, amount, and intensity of rainfall; vegetation type is less significant (Hoffman et al. 1989). Transfer rates of gaseous I2 from the atmosphere are largely constant across plant species (Nakamura & Ohmomo 1980; Nakamura & Ohmomo 1984; Nakamura et al. 1986).
Different plant species accumulate iodine at different rates through their roots; leafy vegetables absorb more than fruiting vegetables. Root iodine concentration > leaf > stem; across all tissues cytoplasm concentration > cell wall > organelle (Weng et al. 2008; Weng et al. 2013).
Iodine can be beneficial to plant growth: barley growth increased by C2H3IO2 > I- > IO3- > IO4− (1.0 ppm growth medium). In peas, 1.0 ppm iodine inhibited growth; I- being more toxic than IO3- (Lehr et al. 1958; Pauwels 1961; Umaly & Poel 1971; Weng et al. 2008). Many species, not just rice, can suffer from iodine toxicity (“reclamation Akagare disease”) (Kiferle et al. 2013; Kato et al. 2013).
The xylem transport mechanism (passively from roots in pillars of dead cells) transports iodine, phloem (active transport by living cells from leaves) probably does not (Herrett et al. 1962). I- is more easily absorbed by roots than IO3-. Soil microbes convert IO3- to I- and encourage absorption by roots (Evans & Hammad 1995) (Mackowiak & Grossl 1999). Leaf absorption is also affected by iodine speciation.
Biofortification of plants with iodine has been attempted as an adjunct to iodinated salt (Smoleń & Sady 2011; Kiferle et al. 2013), but few studies take full account of atmospheric deposition and within-plant transfer mechanisms.
Conclusion: The relationship of iodine and plants depends on plant species, iodine species, growth medium concentration, soil type, atmospheric dynamics, and the two plant transport mechanisms. Too many studies are too narrow in focus: greater thought needs to be given to multivariate issues in the relationship of iodine geochemistry to health.
References
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Herrett RA., Hatfield HH, Crosby DG, and Vlitos AJ. Leaf Abscission Induced by the Iodide Ion. Plant Physiology. 1962; 37(3): 358–63.
Hoffman FO, Frank ML, Blaylock BG, et al. Pasture Grass Interception and Retention of 131 I, 7 Be, and Insoluble Microspheres Deposited in Rain. ORNL 6542. Oak Ridge: Oak Ridge National Laboratory, 1989.
Kato S, Wachi T, Yoshihira K, et al. Rice (Oryza Sativa L.) Roots Have Iodate Reduction Activity in Response to Iodine. Frontiers in Plant Science 0213; 4: 227.
Kiferle C, Gonzali S, Holwerda HT, Ibaceta RR, Perata P. Tomato Fruits: A Good Target for Iodine Biofortification. Frontiers in Plant Science. 2013; 4: 205.
Lehr JJ, Wybenga JM, Rosanow M. Iodine as a Micronutrient for Tomatoes. 1. Plant Physiology. 1958; 33(6): 421–27.
Mackowiak CL, Grossl PR. Iodate and Iodide Effects on Iodine Uptake and Partitioning in Rice (Oryza Sativa L.) Grown in Solution Culture. Plant and Soil. 1999; 212(2): 135–43.
Nakamura Y, Ohmomo Y. Factors Used for the Estimation of Gaseous Radioactive Iodine through Intake of Vegetation. I. Uptake of Methyl Iodide by Spinach Leaves’. Health Physics. 1980; 38(3): 307–14.
Nakamura Y, Ohmomo Y. Transfer of Gaseous Iodine to Tradescantia. Journal of Radiation Research 1984; 25: 251–59.
Nakamura Y, Sumiya M, Uchida S, Ohmomo Y. Transfer of Gaseous Iodine to Rice Plants. Journal of Radiation Research. 1986; 27(2): 171–82.
Pauwels GW, Borst FH. Iodine as a Micronutrient for Plants. Plant and Soil. 1961; 14(4): 377–92.
Smoleń S, Sady W. Effect of Iodine Fertilization and Soil Application of Sucrose on the Content of Selected Heavy Metals and Trace Elements in Spinach. Acta Scientiarum Polonorum – Hortorum Cultus. 2011; 10(4): 37–50.
Umaly RC, Poel LW. Effects of Lodine in Various Formulations on the Growth of Barley and Pea Plants in Nutrient Solution Culture. Annals of Botany. 1971; 35(1): 127–31.
Weng, HX, Hong CL, Xia TH, Bao LT, Liu HP, Li DW. Iodine Biofortification of Vegetable plants—An Innovative Method for Iodine Supplementation. Chinese Science Bulletin. 2013; 58(17): 2066–72.
Weng HX, Hong CL, Yan AL et al. Mechanism of Iodine Uptake by Cabbage: Effects of Iodine Species and Where It Is Stored. Biological Trace Element Research. 2008; 125(1): 59–71.
Text written by Dr Alex Stewart (December 2015, updated April 2019).