Environ Geochem Health (2011) 33:389–397 DOI 10.1007/s10653-011-9384-4 ORIGINAL PAPER Does iodine gas released from seaweed contribute to dietary iodine intake? P. P. A. Smyth • R. Burns • R. J. Huang T. Hoffman • K. Mullan • U. Graham • K. Seitz • U. Platt • C. O’Dowd • Received: 28 June 2010 / Accepted: 11 January 2011 / Published online: 23 March 2011 Ó Springer Science+Business Media B.V. 2011 Abstract Thyroid hormone levels sufficient for brain development and normal metabolism require a minimal supply of iodine, mainly dietary. Living near the sea may confer advantages for iodine intake. Iodine (I2) gas released from seaweeds may, through respiration, supply a significant fraction of daily iodine requirements. Gaseous iodine released over seaweed beds was measured by a new gas chromatography–mass spectrometry (GC–MS)-based method and iodine intake assessed by measuring urinary iodine (UI) excretion. Urine samples were obtained from female schoolchildren living in coastal seaweed rich and low seaweed P. P. A. Smyth (&) C. O’Dowd School of Physics and Environmental Change Institute, National University of Ireland, Galway, Ireland e-mail: [email protected] P. P. A. Smyth R. Burns UCD School of Medicine and Medical Science, University College Dublin, Dublin, Ireland R. J. Huang T. Hoffman Institute of Inorganic and Analytical Chemistry, Johannes Gutenberg University of Mainz, Duesbergweg 10-14, 55128 Mainz, Germany abundance and inland areas of Ireland. Median I2 ranged 154–905 pg/L (daytime downwind), with higher values (*1,287 pg/L) on still nights, 1,145–3,132 pg/L (over seaweed). A rough estimate of daily gaseous iodine intake in coastal areas, based upon an arbitrary respiration of 10,000L, ranged from 1 to 20 lg/day. Despite this relatively low potential I2 intake, UI in populations living near a seaweed hotspot were much higher than in lower abundance seaweed coastal or inland areas (158, 71 and 58 lg/L, respectively). Higher values[150 lg/L were observed in 45.6% of (seaweed rich), 3.6% (lower seaweed), 2.3% (inland)) supporting the hypothesis that iodine intake in coastal regions may be dependent on seaweed abundance rather than proximity to the sea. The findings do not exclude the possibility of a significant role for iodine inhalation in influencing iodine status. Despite lacking iodized salt, coastal communities in seaweed-rich areas can maintain an adequate iodine supply. This observation brings new meaning to the expression ‘‘Sea air is good for you!’’ Keywords Atmospheric gaseous iodine Thyroid Urinary iodine Seaweed Iodine K. Mullan U. Graham Royal Victoria Hospital, Belfast, N. Ireland Introduction K. Seitz U. Platt Institute of Environmental Physics, University of Heidelberg, Im Neuenheimer Feld 229, 69120 Heidelberg, Germany The thyroid hormones thyroxine (T4) and triiodothyronine (T3) play a vital role in human development and metabolism. Iodine forms a major constituent of 123 390 these hormones (65.3% by weight of T4). A regular source of iodine intake, principally dietary, is necessary to maintain normal function in all mammals including humans. Although seawater is relatively poor in iodine (approx. 58 lg/L; Fuge and Johnson 1986), its massive abundance makes it and forms of life of marine origin such as seafish, shellfish, and seaweeds the richest source of iodine on the planet. In dietary terms, the most efficient source of iodine intake is the use of table salt or salt used in food processing of NaCl which has been fortified with KI or KI03 at a level of 20–40 mg/kg (iodized salt). Daily intakes of iodine recommended by the WHO range from 90 lg in infants to 250 lg in pregnant women with adults requiring 150 lg/day. The use of iodized salt (universal salt iodization: USI) is the means of iodine prophylaxis recommended by the WHO (WHO 2007). However, the policy is not practiced by all countries, and in those in which salt iodization is available, it is often on a voluntary basis, giving rise to wide variations in usage. The use of seaweeds in cooking, particularly Japanese and Korean, results in populations in those countries having extremely high dietary iodine intakes. Japanese iodine intake has been estimated at about 1 mg/day (Nagataki 2008), compared with approximately 100 lg/day in European countries (WHO 2007). Seaweeds have also been used as agricultural fertilizers resulting in crops of high iodine content. For example, in Northern Ireland commercial and local harvesting of seaweed and its application as a fertilizer on agricultural soils may in the past have contributed significant concentrations of marine-sourced iodine to coastal soils. Seaweed has also been used as a livestock feed in Irish coastal communities and is often sold for human consumption, commonly known as ‘dulse’ (Smyth and Johnson 2010). However, apart from their occasional use as fashionable health and cosmetic additives, it is doubtful if current seaweed consumption makes a significant contribution to dietary iodine intake. Since molecular iodine (I2) was suggested to be the dominant source of coastal reactive iodine in the marine boundary layer during the 2002 North Atlantic Marine Boundary Layer Experiment (NAMBLEX) field campaign at Mace Head (Ireland) (Saiz-Lopez and Plane 2004), it has become well established by laboratory studies that the emission of this molecular iodine from low tidal macroalgal exposure is indeed a 123 Environ Geochem Health (2011) 33:389–397 most important process responsible for the observed tropospheric iodine level (McFiggans et al. 2004; Küpper et al. 2008). A diagram depicting the ocean– atmosphere–land part of the iodine cycle (Johnson 2003) is shown in Fig. 1. Significant levels of molecular iodine have been observed at Mace Head and nearby sites (*100 parts per trillion (ppt) or *1,000 pg/L) (Saiz-Lopez and Plane 2004; Saiz-Lopez et al. 2006; Peters et al. 2005), and at La Jolla, California (*80 pg/ L) (Finley and Saltzman 2008). While most of the above studies have been located at Mace Head, it should be noted that Mace Head possesses perhaps the lowest algal biomass in the region as most of the shore is characterized by bare rocks rather than notable kelp beds. This study extends the studies at Mace Head to simultaneous measurements in a nearby algal biomass hotspot, Mweenish Bay where seaweed abundance of 1–5 kg/ M2 has been recorded (Sellegri et al. 2005). During a sampling campaign in August and September, 2007, elevated concentrations of I2 were observed in the atmosphere, particularly over the exposed seaweed beds (Huang and Hoffmann 2009; Huang et al. 2010a, b). What is less well known is the extent to which gaseous iodine released from seaweeds could contribute to dietary iodine intake through respiration particularly in populations residing in coastal areas. There are few studies on this subject, but Vought et al. (1964) reported atmospheric gaseous iodine at levels of 0–7.4 lg/m3 which they calculated on the basis of a concentration of 5 lg/m3 would provide an iodine intake of 100 lg/day approaching the 150 lg WHO recommended figure. On the other hand, Johnson (2003) has postulated an intake of 0.3 lg/day from breathed air based on an air intake of 20 m3 per day (Vought et al. 1970) and average atmosphere iodine content of 10–20 ng/m3 (Whitehead 1984). However, one of these authors (Vought et al. 1970) emphasized that much of the discrepancies in accounts of iodine in the atmosphere could be attribute to poor sampling methods. It has also been established by Morgan et al. (1968), in probably never to be repeated experiments involving human volunteers breathing in radioactive I2 gas, that the earliest and most important site for inspired I2 deposition was the nasopharyngeal passage. An important feature of I2 inspiration might be improved bioavailability from the lungs to the bloodstream in contrast to potential losses via the gastric Environ Geochem Health (2011) 33:389–397 391 Fig. 1 The ocean– atmosphere–land part of the iodine cycle updated from Fuge (1996). Reprinted from Johnson (2003) with permission route (e.g. malabsorption, fecal loss). However, such pathways are unproven. It has long been assumed that populations residing near the sea would enjoy superior iodine nutrition compared with those in inland areas primarily due to the consumption of marine-environment foodstuffs. However, iodine deficiency has been demonstrated to exist even in coastal communities on the Portuguese Atlantic islands of Madeira and the Azores (Limbert et al. 2010) with median UI values being lower than on the Portuguese mainland. These islands support very little seaweed growth (Limbert, Private Communication). It is the objective of this study to test the hypothesis that gaseous iodine measured in seaweedrich coastal ‘‘hotspots’’ contributes significantly to iodine intake, as assessed by urinary iodine (UI) excretion, in comparison with coastal areas with lessabundant seaweed growth or inland areas. Subjects and methods Study populations Subjects studied were female schoolchildren (aged \15 years) attending schools in areas of both the Republic of Ireland and Northern Ireland. Areas selected are shown in the accompanying map (Fig. 2). Informed consent was obtained from children, parents, and teachers. The study was carried out with collaboration of the Section of Primary, Community & Continuing Care, Health Services West, Ireland. Subjects (N) were subdivided into groups on the basis both of proximity to the sea and local seaweed abundance: Group A (N = 93): Inland, Rochfortbridge, Co Westmeath: [100 km from the coast. Group B (N = 28): North Coast (Irish Sea; lesser seaweed abundance) Ballycastle, Co Antrim, within 10 km of the coast. Group C (N = 46): West Coast, Seaweed Hotspot, Carna, Co Galway. In general, the Atlantic West coast of Ireland displays the greatest abundance of seaweed growth (Hession et al. 1998). The seaweed hotspot at Mweenish Bay adjacent to Carna and the marine Research Station at Mace Head has been used in many experiments on iodine release by seaweeds (Huang et al. 2010a, b). This is an area of high seaweed density being a sheltered bay where seaweeds can readily attach to rocks (Fig. 3). Seaweed density is in the region of 1–5 kg/m2 (Sellegri et al. 2005). It should be noted that exposure to extensive wave action can reduce the abundance or even occurrence of kelp (Hession et al. 1998). Ballycastle, Co Antrim, an area with a long tradition of kelp harvesting, lies on the more exposed Northern Irish Coast where seaweed beds might be expected to produce and maintain less iodine vapor. 123 392 Environ Geochem Health (2011) 33:389–397 Fig. 2 Map of Ireland, showing sites where urine samples were collected from schoolchildren. Group A (N = 93): Inland, Rochfortbridge, Co Westmeath: [100 km from the coast. Group B (N = 28): North Coast (Irish Sea; lesser seaweed abundance) Ballycastle, Co Antrim: within 10 km of the coast. Group C (N = 46): West Coast (Coastal; seaweed hotspot), Carna, Co Galway: on coast Fig. 3 Mweenish Bay, Co Galway, Ireland. Seaweed hotspot Methods Atmospheric molecular iodine (I2) The field measurements of I2 in the atmosphere were made at the Mace Head Atmospheric Research Station 123 (53.32o N, 9.90o W) and Mweenish Bay (53.31o N, 9.83o W), in Co. Galway Ireland. The latter is located about 7 km southeast of the Mace Head research station. Measurements were made between 6th August and the 4th of September 2007 (Huang et al. 2010a). Molecular iodine (I2) was measured by a diffusion denuder system in combination with a gas chromatography–mass spectrometry (GC–MS) method, which provides ‘‘single-point’’ in situ concentrations of I2 at the sampling site (Huang and Hoffmann 2009). The diffusion denuder can separate gases and particles in the same air mass and quantitatively collect gaseous I2 by the formation of inclusion complex between the trapped I2 and the denuder coating materials á-cyclodextrin/129I- (Huang and Hoffmann 2009; Huang et al. 2010a, b). Since I2 is rapidly photolyzed to iodine atoms during daytime, the denuder tubes were set up directly above the algal beds with a very short vertical distance of around 5 cm between the seaweed and the denuder inlet to minimize the potential influence of photolysis. The denuder method Environ Geochem Health (2011) 33:389–397 393 has also been used to detect iodine species other than I2 including reactive iodine species HOI and ICI (Huang and Hoffmann 2009). Measurements were made between 7th August and 27th August, 2007 (Huang et al. 2010b). Urinary iodine excretion Urinary iodine (UI) was measured using the ammonium persulfate digestion microplate method followed by Sandell-Kolthoff colorimetry as described by Ohashi et al. (2000). This method measures total iodine in urine. Results were expressed as lgI/L urine (lg/L). Quality control was assessed under the Centre for Disease Control (CDC, Atlanta, Georgia, USA) EQUIP (Ensuring the Quality of Urinary Iodine Procedures) programme (Caldwell et al. 2005). Study group values were expressed as medians and percentage of individual values indicative of iodine deficiency (\50ug/L) or higher iodine intake ([150 lg/L) as recommended by the WHO (2007). Statistical analysis was performed using Wilcoxon’s rank sum test for unpaired samples and the chi squared test (Fischer’s exact test). Results Figure 4 shows daytime I2 values (pg/L) measured in Mweenish Bay over the seaweed bed (hotspot) and 150 m downwind. Measurements were taken in five inconsecutive days over a campaign period of 30 days, and as shown, the I2 values measured over the hotspot varied from 1,145 to 3,132 pg/L during this period. Much lower values were observed at the site 150 m downwind of the seaweed bed where I2 ranged 155–905 pg/L. The variations observed in Fig. 4 could be attributed to the properties of different seaweeds or the surrounding atmosphere (Huang et al. 2010). Since the inlet of the denuder was set up very close to the seaweed beds (*5 cm) during sampling, it is reasonable to treat these data as local source strength. This significant decrease of I2 mixing ratio observed downwind of (i.e. further away from) the seaweed beds could be attributed to the rapid photolysis of I2 that has a photolytic lifetime of 10 s (Saiz-Lopez et al. 2006). Note that during these measurements, the wind (from sea direction) passed over the seaweed beds with a speed of 3.7–7.7 m s-1 Fig. 4 Gaseous I2 measured by a diffusion denuder system in combination with a gas chromatography–mass spectrometry (GC–MS) method, which provides ‘‘single-point’’ in situ concentrations of I2 at the sampling site (Huang and Hoffmann 2009). Measurements taken in daylight at low tide over, and 150 m downwind of, the Mweenish Bay seaweed hotspot corresponding to a transport time of about 20–41 s. Wind directions and speeds were as follows:- 07/08/ 2007, 299°, speed 6.1 m/s; 08/08/2007, 198°, speed 7.4 m/s; 15/08/2007, 330°, speed 7.7 m/s; 22/08/ 2007, 316°, speed 6.8 m/s; 27/08/2007, 342°, speed 3.7 m/s. Therefore, during the 5-day measurements, the winds were almost blowing from northwest, except on 8th Aug (southwest). In all cases, the winds passed over seaweed beds before reaching the sampling point. However, the averaged night-time I2 mixing ratio downwind of the seaweed beds (*1,287 pg/L) is comparable to the levels found directly above the seaweed beds (source strength), although the values drop to around * 300 pg/L in several episodes. A mixing ratio is defined as that concentration in which one molecule of species is present per one million molecules of air. As suggested by Huang et al. 2010b, coastal background I2 mixing ratios of 156–187 pg/L could be maintained even in the face of strong ([10.8 m s-1) westerly winds (i.e. from the sea). Figure 5 shows the relationship of sampling time (day v night) and tidal height to I2 released at 150 m downwind of the seaweed bed. The maximum tidal heights related to these data ranged from 0.5to 3.8 m. The two factors, time and tidal height, combine to produce the lowest values in daytime samples (58–464 pg/L). As shown in Fig. 5, the combination 123 394 Environ Geochem Health (2011) 33:389–397 Fig. 5 Influence of time (Nighttime (closed circle) Daytime (open circle)) and tidal height on atmospheric I2 measured 150 m downwind of a seaweed hotspot at Mweenish Bay. Note different scales on nighttime and daytime axes Table 1 Possible contribution of atmospheric I2 to daily iodine requirements Approx. average I2 lg inspired/24 h Sampling time and location Atmospheric I2 pg/L (range) Daytime 381 (155–905) Still night 1287 12.8 Over seaweed mass 1934 (1145–3132) 19.6 (11.5–31.3) Coastline background 155–186 3.8 (1.5–9.0) 1.5–1.8 Amount of I2 inspired arbitrarily set at 10,000 L/day Adapted from Huang et al. (2010a). Atmos. Chem. Phys. 10. 4823–4833 of nighttime with the lowest tide (0.5 m) gave the highest atmospheric I2 values (1,150 and 2,000 pg/L). In contrast, the apparent absence of photolysis (i.e. chemical changes brought about by the influence of light) of I2 in nighttime samples gave values of up to orders of magnitude higher (121–2,006 pg/L). As expected, lowest values were seen at high tide when the seaweed was covered and therefore subject to less stress. Table 1 shows an approximation of possible iodine intake from inspired gaseous I2. Calculations are based on the average I2 (pg/L) and an assumed daily respiration of 10,000 L of air. This is a resting level which would be significantly increased during vigorous exercise. Using a daily intake of 10,000 L of air, the calculated daily intake on the basis of atmospheric I2 levels would range from 3.8 to 19.6 lg/day. This would be significantly diminished further away from 123 Fig. 6 Urinary iodine (UI) excretion expressed as median (lg/ L) and % of values \50 and [150 lg/L in the three groups of female schoolchildren. Group A (inland); Group B (Coastal, lesser seaweed abundance); Group C (Coastal, seaweed hotspot) the seaweed bed. Inland measurements were not taken at this time. At an ambient coastal background level of 155–186 pg/L, it would only amount to a daily intake of approximately 1–2 lg. Even using a daily air intake of 2,000L (Vought et al. 1970) would only increase iodine inhalation at ambient coastal background to 2–4ug. However, it is known that children have higher respiration rates (California EPA Research Note 1994), which can result in their greater exposure to pollutants and perhaps to iodine (Bateson and Schwartz 2008). The calculated iodine intakes shown in Table 1 are not very significant in terms of the WHO recommended intake of 150 lg/day. However, it does not take account of vigorous exercise, where air intake could be several multiples of resting intake (California Environmental Protection Agency 1994), or indeed of possible greater bioavailability of lung rather than gastric absorption. The distribution of urinary iodine excretion in different study populations is shown in Fig. 6. The highest median UI (158 lg/L; Range 30–567 lg/L) occurred in Group C, residing near the seaweed hotspot. This value was significantly higher than those of 71 lg/L (range 31–175) and 58 lg/L (range 40–303) in Groups A and B (p \ 0.01 in each case). These findings were reflected in the number of values indicative of iodine deficiency (\50 g/L) which amounted to 8.7% in Group C but reached 14.5% in Group B and was highly significantly elevated (37.6%) in the inland population (Group A) (p \ 0.01). In contrast, higher UI values ([150ug/L) predominated Environ Geochem Health (2011) 33:389–397 in Group C (45.6% v 3.6% and 2.3% in Groups B and A) (p \ 0.01). Discussion The use of the diffusion denuder system in combination with GC–MS measurement has demonstrated substantially higher levels of gaseous I2 over seaweed beds than was hitherto reported (Saiz-Lopez and Plane 2004; McFiggans et al. 2004; O’Dowd and Hoffmann 2005; Sellegri et al. 2005; Pirjola et al. 2005). As the values recorded in the present study were single point in situ measurements, not surprisingly the highest values were observed over the seaweed beds with lower values downwind. The results obtained were of course highly variable being dependent on wind direction and strength as well as time of sampling (day v night) and tidal height. The gaseous I2 levels recorded varied from a coastal background low of 155 pg/L to a high over the seaweed mass of 3,132 pg/L. Attempts to apply these values to potential ingestion by humans are fraught with difficulty. It could be argued that the majority of people reside somewhat inland from the coast and therefore would only be exposed to coastal background I2 levels. On the basis of breathing in an arbitrary daily 10,000L of air, only 1–2 lg of I2 would be ingested even in coastal areas which in terms of the WHO recommended 150 lg/day (WHO 2007) would be inconsequential even in an area of borderline dietary iodine intake such as Ireland (Nawoor et al. 2006; Lazarus and Smyth 2008). This may indeed be the case, but the possibility of exposure to much higher seaweed derived I2 levels cannot be ignored. A much higher contribution of atmospheric I2 (*100 lg/day) was suggested by Vought et al. (1964). However, the higher atmospheric values potentially yielding a dietary intake of up to 30 lg/day could if inhaled make a significant contribution, particularly in the context of an estimated average requirement (EAR) of 95 lg/day (Zimmermann 2009). A major difficulty in assessing such exposure are the many factors which could affect seaweed derived atmospheric I2. In addition to wind direction and strength, time of sampling and tidal height previously mentioned, density and seaweed species differences in iodine content and bioavailability could determine how much gaseous I2 was available 395 for ingestion. Firstly, there is almost certainly a difference between the coastal and inland atmospheric iodine backgrounds with iodine levels presumably declining with distance from the sea. Unfortunately in this study, inland atmospheric iodine was not measured. One method of deposition would be ingestion of sea spray which could potentially equal or exceed gaseous iodine. However, even allowing for inhalation of large amounts of sea spray through ingestion, unlikely during the calm periods of study, an increment over gaseous iodine of significant magnitude to alter iodine nutrition does not seem probable. The efficiency of the lung in absorbing gaseous I2 remains uncertain. The earlier work of Morgan et al. (1968) suggested deposition of particle-associated I2 in the nasopharyngeal tract as the major source of ingestion. As the sodium iodide transporter NIS has only rarely been demonstrated in lung tissue (Spitzweg et al. 1998; Harun-Or-Rashid et al. 2010), deposition may indeed be the most efficient pathway. However, more recent work by Harvey et al. (2006; Harvey 2009) documented differences in gas uptake from that occurring as a result of particle deposition. In particular, the inhalation dose coefficient (DC) is much greater in younger age groups (Harvey et al. 2006) supporting findings in the present study conducted in girls aged less than 15 years. This is consistent with the evidence that children have greater rates of inhalation than do adults (California Environmental Protection Agency 1994; Bateson and Schwartz 2008). However, in view of the very low atmospheric I2 recorded, it must be emphasized that some extremely preferential I2 absorption by the lungs would be necessary to make a significant contribution to daily iodine intake. On the other hand, such a contribution would be proportionally greater when iodine intake from other sources was restricted as in individuals with low UI (\50 lg/L). Despite the apparently low potential contribution of seaweed-derived gaseous I2 to daily iodine intake, the findings that median UI and % of lower and higher values in the three study groups A-C were consistent with the presence of a seaweed mass support some form of marine related iodine intake. Particularly noteworthy was the finding that 45.6% of female children living adjacent to the seaweed hotspot had UI [ 150 lg/L compared with 3.6% in the coastal area with lesser seaweed abundance and 2.3% in an inland community. It is of 123 396 course possible that some undetected dietary preference of the Group C children contributed to the finding particularly in view of the large range of UI values encountered in all three study groups. However, there was no evidence of such an intake. A wide distribution of UI values is characteristic of this mode of investigating iodine status, since it reflects iodine intake over the previous 24 h rather than long-term intake (WHO 2007; Zimmermann 2009). For this reason, the distribution of low (\50 lg/L) and high ([150 lg/L) UI values as shown in this study provides a useful index of iodine status. Regional differences in food intake might in the past have provided a satisfactory explanation for variance in dietary intake when food consumed was almost exclusively locally sourced, but is less likely in the era of supermarkets with widely sourced products. It is unclear from the results in this study if the iodine content of air, ingested by respiration, makes a significant contribution to overall daily iodine intake in populations living near to, in comparison with remote from, the sea. Interestingly Limbert et al. (2010) reported on UI levels being lower on the Azores and Madeira Islands where it might be expected that iodine intake would be higher in populations residing near the sea than in continental Portugal. As previously stated, these islands have a very low seaweed abundance. This finding is supportive of the hypothesis that iodine intake in coastal regions may be dependent on seaweed abundance rather than simply proximity to the sea. Certainly larger studies with greater control of dietary input and the form of iodine inhalation would add weight to the hypothesis as would a better understanding of the efficiency of lung absorption of seaweed-derived iodine. Nonetheless the findings do not exclude the possibility of a significant role for iodine inhalation in influencing iodine status and may help explain why despite the absence of a regular source of dietary iodine intake such as iodized salt, coastal communities residing in seaweed-rich areas can maintain an adequate dietary iodine supply. This observation may bring new meaning to the expression ‘‘sea air is good for you’’. Acknowledgments The authors gratefully acknowledge the cooperation of the parents and schoolchildren of participating schools in both the Republic of Ireland and Northern Ireland. We greatly appreciate the assistance of the HSE, West, Dr Karla Kyne, Area Community Medical Officer for the Carna 123 Environ Geochem Health (2011) 33:389–397 Area, Dr Mary FitzGerald, Senior Medical Officer Primary, Community & Continuing Care. Dr John O’Donnell of Galway and Richard Fitzgerald of the Martin Ryan Institute, NUI, Galway. 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