Abstract
Background:
Production of iodized salt in Iran for household consumption began in 1990. Previous studies have reported sustainable elimination of iodine deficiency disorders in Iran. The aim of this study was to evaluate the iodine nutritional status in Tehran in 2009.
Methods:
In this cross-sectional study, 383 Tehranian households were enrolled through randomized cluster sampling and a total of 639 adult subjects (242 men and 397 women), aged 19 and over, participated. A 24-hour urine sample was collected for measurement of urinary iodine, sodium, and creatinine concentrations using the digestion method, flame photometry, and autoanalyzer assay, respectively. Salt intake was estimated and iodine content of household salt was measured by titration.
Results:
Median (interquartile range) iodine content of household salt and urinary iodine concentration (UIC) in Tehran were 21.2 (3.2–31.7) parts per million and 70.0 (34.0–131.2) μg/L, respectively. There was no statistically significant difference in 24-hour UICs between men and women. Median (interquartile range) daily salt intake was 7.6 (5.5–9.8) g, which was not different in the two genders. According to the WHO/ICCIDD/UNICEF classification, 11.2%, 25.9%, 26.7%, 25.1%, 8.0%, and 3.2% of participants had UIC <20, 20–49, 50–99, 100–199, 200–299, and >300 μg/L, respectively.
Conclusions:
Mild iodine deficiency has recurred in Tehranians. The results emphasize the need for continuous monitoring in all regions, even in a country with iodine sufficiency.
Introduction
Data from several countries indicate that lack of a well-monitored salt iodization (SI) program is accompanied by recurrence of iodine deficiency (5 –9). As seen in Azerbaijan, Kazakhstan, Kyrgyzstan, Guatemala, Thailand, Brazil, Colombia, and Mexico, failure of monitoring in any previously successful program may result in recurrence of iodine deficiency (6,7,9 –12). Moreover, downward trend of urinary iodine concentration (UIC) has been observed in some developed countries such as the United States between National Health and Nutrition Examination Surveys I and III, and New Zealand and Australia (13 –15); reemergence of iodine deficiency has been reported in the two latter industrialized countries, previously iodine sufficient (16 –20). The reasons for decreased UIC has been ascribed to lack of supervision and monitoring, reduction in iodine content of milk and dairy products, removal of iodate dough conditioners in commercial bread, recommendation for reduced salt intake to prevent hypertension and chronic diseases, and increased use of noniodized salt in convenience foods (13,21 –23).
The Islamic Republic of Iran had been recognized as an area of iodine deficiency (24,25) and since 1990 a comprehensive national program for elimination of iodine deficiency is in place. Mandatory production of iodized salt with 40 parts per million (ppm) iodine concentration for household consumption was begun in 1994 and since that time over 90% of households consume iodized salt. Although three nationwide surveys on monitoring of iodine nutrition have shown sustainable elimination of iodine deficiency disorders (IDD) in schoolchildren (26,27), a recent unpublished report in 2007 demonstrated that despite reduction of goiter rate to below 6.5%, the median UIC had decreased when compared with 2001.
In Iran, iodized salt is the main dietary iodine source, and hence, information on contribution of iodine by iodized salt is necessary for evaluation of the dietary iodine status. The aim of this study was to evaluate iodine nutritional status of Tehranians through measurement of 24-hour urine iodine excretion, estimation of salt intake, and assessment of salt iodine content.
Materials and Methods
Subjects
In this cross-sectional study, the Tehran city map was divided into four distinct areas, that is, the south, west, east, and north. In each region, two locations were randomly selected and the nearest health care centers of each location were assigned. In each health care center, 40 households in the form of five clusters, each including 8 households, were chosen for the study. During home visits, the researcher clarified purpose and methodology of the study and asked two individuals of each household, the lady and a second adult person, to participate in this study. Of a total of 321 households initially enrolled for the study, 7 households provided only salt samples, but abstained from urine collection, and of 55 households only one member participated. Based on the targeted sample size, in proportion to missing subjects, 55 additional households with two participants were added. Hence, eventually 383 households, including the 7 households (only salt samples), the 321 households (55 with one participant), and 55 additional households with two participants (for urine collection), collaborated in this study. Following exclusion of pregnant and lactating mothers (n = 24), and participants with incomplete urine samples (n = 34), overall, 639 adults (age ≥19 years) remained for the current analysis. Informed consent was obtained from each household. Personal information, family and personal history of thyroid disease and hypertension, and information on consumption of medications and iodine-containing supplements were obtained and documented using an interviewer-administered questionnaire.
Salt sample collection
During the first home visit, two tablespoon salt samples were collected from each of the 383 households. Some households used two types of salt, for which samples of both were collected. The samples were kept in lightproof and closed plastic cans and labeled with the code of each household. The average iodine content of salt was reported for households with two samples.
Urine collection
At the first home visit, written instructions and labeled 2.5-L plastic containers were distributed to the lady and second adult of each household who were asked to collect all urine passed during a 24-hour period, beginning on Friday (weekend day in Iran) starting from the second morning urine and ending with the first urine passed the following morning.
At the second visit, on the following Saturday, all samples were collected and sent to the iodine laboratory of the Endocrine Research Center, the reference laboratory of eastern Mediterranean region; total volume was measured and urine was transferred in screw-top labeled plastic vials. The aliquots were kept frozen until iodine, sodium, and creatinine measurements.
Salt intake estimation
After collection of 24-hour urine samples, for estimation of daily salt consumption, every household received an accurately weighed and labeled salt package to use consecutively for 15 days. If the number of persons in each household was over four individuals, two salt packages were given. The mother of each household was instructed to use the salt during food preparation as well as for table salt. At the third visit on the 15th day, the leftover salt in each household was reweighed and total salt consumption was calculated. Salt was weighed at the beginning and end of study on a scale with 0.1 g sensitivity and expressed as grams per day.
Laboratory measurements
Iodine concentration of salt samples was determined using the iodometric titration method with 1 ppm sensitivity and 1% coefficient of variation (28). The obtained values were shown in ppm. Iodine concentration in urine sample was analyzed using the Sandell-Kolthoff (acid-digestion) reaction (29) and results were expressed as micrograms of iodine per liter of urine. The intra- and interassay coefficients of variation were 9.6% and 10.4%, respectively, and the sensitivity was 2 μg/L. Completion of 24-hour urine sample collection was confirmed with creatinine concentration. Urine samples with creatinine levels below 500 mg/day were considered incomplete. Urinary creatinine was measured by the kinetic Jaffé method (creatinine colorimetric kit; Pars Azmoun). The assays were run with an autoanalyzer (Vitalab, Selectra-2). The assay sensitivity and coefficient of variation were 0.2 mg/dL and 2.1%. Sodium excretion in 24-hour urine collections was analyzed by emission flame photometry (Corning 480).
Definition of terms
Salt intake was estimated by 24-hour urinary sodium excretion (1 g salt was equal to 17.1 mmol sodium) (30 –32). Per capita salt consumption was calculated based on amount of salt consumed per person per day in a household (33 –35). According to WHO/ICCIDD/UNICEF criteria, median UICs <20, 20–49, and 50–99 μg/L were representative of severe, moderate, and mild iodine deficiency, respectively. Median UIC values 100–199, 200–299, and ≥300 μg/L were considered as adequate, more than adequate, and excessive, respectively (2,36).
Statistical analyses
Frequency distribution (%) and mean ± standard deviation (SD) were computed according to qualitative and continuous numerical variables. Depending on normality of variables, categorical variables were compared by Mann–Whitney and Kruskal–Wallis tests. Differences between the four regions were determined by post hoc (Bonferroni adjustment) test. Univariate and multiple logistic regression were used to identify influence factor(s) associated to UIC <100 μg/L. Statistical analyses were done using SPSS version 15 software package, with p < 0.05 being considered as significant.
Results
Three hundred eighty-three households inclusive of 639 adults, 397 (62.1%) women and 242 (37.9%) men, with a mean age of 42.8 ± 13.1 years, completed the study. Basic characteristics of participants in different regions of Tehran are shown in Table 1. No significant difference in the basic variables among participants of these four regions was observed.
Kruskal–Wallis test shows no significant difference in basic characteristics of participants in the four regions of Tehran.
UIC values
UIC was measured in 639 persons who had adequate urine collection. Mean ± SD and median (interquartile range [IQR]) of 24-hour UICs in Tehran were 97.6 ± 82.9, and 70.0 (34.0–131.2) μg/L, respectively. Data on 24-hour UIC levels in different regions of Tehran are presented in Table 2. According to the WHO/ICCIDD/UNICEF classification, 11.3%, 25.8%, 26.6%, 25.0%, 8.2%, and 3.1% of participants had UIC <20, 20–49, 50–99, 100–199, 200–299, and >300 μg/L, respectively. Table 3 shows median (IQR) 24-hour UICs in different regions of Tehran. Median (IQR) 24-hour UIC was 49.0 (30.0–86.5), 76.0 (34.0–153.0), 69.0 (31.5–116.5), and 102.2 (47.5–166.8) μg/L in the south, west, east, and north regions of Tehran, respectively. We found a significant difference in 24-hour UIC between the four regions of Tehran (p < 0.05). Post hoc test showed statistically significant difference in 24-hour UICs between the south and west. Also, a significant difference was found between north and east of Tehran (p < 0.001). Values for mean ± SD and median (IQR) 24-hour UIC in men (n = 242) were 103.4 ± 91.0 and 72.9 (37.0–136.1) μg/L and in women (n = 397) were 94.2 ± 77.5 and 68.6 (33.0–128.0) μg/L, respectively. No statistically significant differences were found in the 24-hour UICs among different age groups and two genders.
Values are given in percentages.
UIC, urinary iodine concentration.
Kruskal–Wallis test shows significant difference in 24-hour UIC, salt intake, salt per capita, and iodine content of salt in the four regions of Tehran.
Mann–Whitney U-test shows no significant difference in 24-hour UIC, salt intake, salt per capita, and iodine content of salt between the two genders.
Significant difference in comparison to the west of Tehran.
Significant difference in comparison to the north of Tehran.
ppm, parts per million.
Salt intake estimation
Mean ± SD and median (IQR) per capita daily salt consumption were 9.5 ± 5.1 and 8.4 (5.7–12.2) g, respectively. The median (IQR) per capita daily salt consumption was 9.1 (6.6–12.8), 7.6 (5.6–11.1), 9.5 (6.7–13.3), and 6.7 (4.9–12.2) g in the south, west, east, and north of Tehran, respectively. Mean ± SD and median (IQR) daily salt intake were 8.0 ± 3.3 and 7.6 (5.5–9.8) g, respectively. Median (IQR) daily salt intake was 7.7 (5.6–9.8), 8.5 (6.1–10.6), 7.3 (5.4–9.5), and 7.1 (5.4–9.8) g in the south, west, east, and north of Tehran, respectively. There were statistically significant differences in per capita salt consumption and daily salt intake between the four regions of Tehran (p < 0.05). The results of post hoc test showed no statistically significant difference in per capita salt consumption between the south and east of Tehran, whereas the other pairwise comparisons were significant (p < 0.001). There was significant difference in salt intake between west and north of Tehran (p < 0.01). Mean ± SD daily salt intake was 8.2 ± 3.6 g in men and 7.9 ± 3.2 g in women, with no statistically significant difference between the two genders.
Iodine content of the salt
Mean ± SD and median (IQR) iodine content of salt samples were 19.8 ± 14.9 and 21.2 (3.2–31.7) ppm, respectively. The proportion of salts with iodine content <10, 10–20, 20–40, and >40 ppm in different regions of Tehran is presented in Table 4. Frequency distributions of salts with iodine content of <10, 10–20, 20–40, and >40 ppm were 36.8%, 11.7%, 46.3%, and 7.8%, respectively. Median salt iodine content was <10 ppm in the south and east, whereas it was >20 ppm in the west and north of Tehran. We found statistically significant difference in iodine content of salt among different regions of Tehran (p < 0.001). No significant difference was observed in iodine content of salt between the south and east of Tehran, whereas the other pairwise comparisons were significant (p < 0.001).
Values are given in percentages.
Overall, UIC <100 and >100 μg/L were present in 408 (63.8%) and 231 (36.2%) participants, respectively. There were statistically significant differences in salt intake and iodine content of salt between these subgroups (p < 0.05). Median UIC was <100 μg/L in the south, west, and east, whereas it was >100 μg/L in the north of Tehran. In the south, east, and west of Tehran, median iodine contents of salt and salt intake were 3.2, 8.5, and 21.9 ppm and 7.7, 7.3, and 8.5 g per day, in regions with UIC <100 μg/L, respectively. With respect to the amount of salt intake and iodine content of salt, median daily iodine intake was 26.5 and 54.1 μg in the south and east (well below the 150 μg per day recommended dietary allowance), whereas it was 158.0 and 220.0 μg in the west and north of Tehran. Significant correlations were observed between iodine content of salt (r = 0.47, p < 0.001) and salt intake and with the UIC value (r = 0.12, p < 0.001).
The results of univariate and multiple logistic regressions are shown in Table 5. In the multivariate adjusted model, lower salt intake quartiles increased risk of UIC <100 μg/L when compared with higher quartiles. Risk of UIC <100 μg/L in the lowest salt iodine quartile was 8.14-fold greater than the highest quartile (95% confidence interval, 4.35–15.23). There was no statistically significant association between age, sex, education, and UIC values <100 μg/L.
CI, confidence interval; Q, quartile.
Discussion
This 2009 cross-sectional study indicates that some inhabitants of Tehran city suffer from mild iodine deficiency. Comparing the three national surveys conducted on monitoring of iodine nutrition, we found that the pattern of UIC values in Tehran had a downward trend. Median UIC in Tehran was 232 μg/L in 1996, 190 μg/L in 2001, and 100 μg/L in 2007, respectively (26,27). Present data confirm that dietary iodine intake has been decreased, which is observed more in the southern region of the city with lower socioeconomic status, when compared with other parts of Tehran. The illegal production and distribution of less-expensive noniodized or inadequately iodized brands of salt is the major destabilizing factor in the south, which is why salts consumed by households in the south of Tehran contain less amount of iodine.
In countries where iodized salt is the only main dietary iodine source, the amount of salt intake and iodine content of the salt are two major determinants of iodine nutritional adequacy (2,36). Based on the WHO/ICCIDD/UNICEF recommendations, to ensure the dietary iodine requirement, salt iodine content should be within the range of 20–40 ppm based on the assumption that salt intake of each individual was 10 g per capita per day. Our findings demonstrated that approximately half of households did not use salt with iodine content >20 ppm. When compared with 1996 and 2001 reports, the proportion of households, using salt with iodine content below 15 ppm, increased in 2007. The study by Azizi et al. in 2001 demonstrated that reduction in UIC level from 1996 to 2001 among Iranian schoolchildren with no alteration in iodine content of salt might be related to environmental and/or dietary factors, for example, use of microwave in food preparation or loss of iodine during poor preservation conditions (27). In some of the Latin American countries such as Argentina, one of the pioneer countries in the use of iodized salt for eradication of IDD in 1952, IDD occurred in some regions in 1980 and 1990, following considerable control of IDD and decrease in goiter rate, because of lack of monitoring and inadequate government support (11). A relapse of IDD also recurred in Guatemala, the Dominican Republic, Haiti, Mexico, Colombia, and Thailand because of lack of standard monitoring of SI programs (7,11). A similar pattern was observed in previous successful programs in some regions of the former Union of Soviet Socialist Republics, Azerbaijan, Kazakhstan, and Kyrgyzstan (7,9,10). Moreover, the study by Rego-Iraera et al. confirmed that ineffective SI program could result in iodine deficiency in adult populations; nevertheless, assessment of schoolchildren showed iodine sufficiency (37). The failure in sustainable iodine supplementation could be explained by a lapse in appropriate monitoring of the SI program following sustainable elimination of IDD.
Certain developed countries have also experienced recurrences of iodine deficiency. Dietary iodine sources vary in different countries. In some developed countries, milk, meat, egg, and baked bread, in addition to iodized salt, are recognized as important sources. In Australia and New Zealand, change in iodine content of food stuffs, infrequent use of iodized salt in households, and increase in noniodized salt use in commercial foods have resulted in the reemergence of iodine deficiency (16,18).
In contrast to European countries where 80% of salt consumed is hidden salt (38,39), in Iran, a significant portion of salt intake comes from iodized salt, used during cooking and as table salt. Considering that nearly all salt intake was from iodized salt, our data illustrated that individuals with daily salt intake of <7.7 g were vulnerable to UIC <100 μg/L. The results obtained supported the WHO/ICCIDD/UNICEF declaration that reduction in salt intake to <10 g per day may influence dietary iodine intake (2,36). In addition, several studies using different methods for determination of discretionary salt intake confirmed our results that decrease in the consumption of iodized salt could affect dietary iodine status (34,35,40,41). Previously, two provincial studies from Isfahan and Ilam showed that daily salt intake was around 10 g in 1998 and 2000 (42,43). A low salt intake among Tehranians can be attributed to public education to reduce salt intake because of high prevalence of noncommunicable diseases, especially cardiovascular disease, in Iran (44).
In this study, salt intake was estimated using two methods. Among Tehranian households, salt used during food preparation was much more than the amount of salt intake (e.g., salt is used in the water to boil vegetables, macaroni, and rice, and most of it is discarded after straining); as a result, 24-hour urinary sodium excretion was a more reliable method (30 –32). A previous study in Iran determined the daily salt intake using the per capita salt consumption method (43) and showed higher daily salt intake; however, overestimation of daily salt intake may have been a result of per capita salt consumption without measuring 24-hour urinary sodium excretion (40,41).
The strength of this research was the 24-hour urine sample collection, which is considered the gold standard and more precise method than the spot urine collection, for the estimation of iodine intake. Yet, a single 24-hour urine sample may also be a poor indicator of habitual iodine intake, because of variation in daily dietary iodine intake (45). Another potential limitation of this study is related to the cross-sectional design of this study that cannot establish causality relationships.
In conclusion, despite Iran still being considered as a country successful in sustainable elimination of IDD over the past 2 decades, mild iodine deficiency has reemerged in some inhabitants of Tehran city, a finding that necessitates more vigorous monitoring of the program of IDD elimination even in countries with all the national indicators of sustainable elimination of iodine deficiency.
Footnotes
Acknowledgments
This study was supported by financial grants from both the Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, and the National Nutrition and Food Technology Research Institute, Faculty of Nutrition and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, Iran. The authors express their appreciation and gratitude to Golaleh Asghari and Maryam Safarkhani for their assistance in statistical analysis of this study and to Ms. Nilufar Shiva for language editing of the manuscript.
Disclosure Statement
None of the authors has any personal or financial conflicts of interest.
