European Journal of Clinical Nutrition (2006) 60, 426–433
& 2006 Nature Publishing Group All rights reserved 0954-3007/06 $30.00
www.nature.com/ejcn
ORIGINAL ARTICLE
Risk factors for goiter in primary school girls in Qom
city of Iran
SM Mousavi1, N Tavakoli2 and F Mardan2
1
Cancer Institute, Cancer Research Center, MAHAK Medical/Rehabilitation Complex, Darabad, Tehran, Iran and 2Fatemieh Medical
University, Qom city, Iran
Objective: Goiter is endemic in Iran. The iodine deficiency disorders program was begun a few years ago in Iran, and the
coverage of iodized salt is sufficient now. But, in a periodic yearly medical examination of primary school girls in Qom, the
prevalence of goiter was above 30% in 2002. This survey was designed to study the risk factors of goiter in those students.
Design: The study was a randomized (multistage, proportional simple random sampling) case–control study.
Subjects and interventions: We selected and performed thyroid examinations in 1050 girl students in primary schools in Qom
city of Iran in 2002. We found 284 cases: girls in primary schools had goiter in accordance with the clinical exam of World Health
Organization classification. Among students who did not present with goiter in the clinical exam, we randomly selected 288
students as the control group. We used a questionnaire to evaluate them for the risk factors of goiter.
Results: The mean7s.d. ages of cases and controls were 8.771.3 and 8.971.3 years, respectively. There is no significant
difference between the two groups regarding history of soya, kale, turnip, fish, daily iodized salt usage, education and job of
mothers, monthly family income, nationality, immigration and residential situation. By using multinomial logistic regression, we
found that storage of iodized salt in open containers, odds ratio (OR): 2.201 (1.412–3.428); P-value o0.0001, medium
socioeconomic situation (SES) of family, OR: 2.099 (1.029–4.282), P-value ¼ 0.041, district 2 of Qom city, OR: 2.880 (1.376–
6.027), P-value ¼ 0.005, and district 3 of Qom city, OR: 2.051(1.032–4.078), P-value ¼ 0.041, were the major risk factors for
goiter in this population.
Conclusions: In this study, the main risk factors for goiter were storage of iodized salt in open containers, medium SES and also
living in specific districts of Qom city. As the coverage of iodinized salt is over 95% in Iran, we advise the education of the family
about storage of iodized salt in closed containers. We also recommend the study of the other risk factors of goiter in the different
geographical areas of Iran, because of differences in the SES and nutritional habits.
Sponsorship: This study was supported by issuing permission letters for our activities: (not funding support) Qom Health
Network and Medical Services, Qom Medical University, Qom Primary School Education Office, Fathemieh Medical University.
European Journal of Clinical Nutrition (2006) 60, 426–433. doi:10.1038/sj.ejcn.1602335; published online 23 November 2005
Keywords: goiter; risk factors; iodized salt storage; Iran
Introduction
Iodine is a mineral substance, which is essential for the
development and growth of the human body. Iodine
deficiency disorders (IDD) affect people before they are born
Correspondence: Dr SM Mousavi, Cancer Institute, Cancer Research Center,
MAHAK Medical/Rehabilitation complex, PO Box 19395-5445, Oshan Blv.
Lashkarak Road, Darabad, Tehran, Iran.
E-mail: [email protected]
Guarantor: SM Mousavi.
Contributors: SMM, NT, and FM.
Received 21 October 2004; revised 19 September 2005; accepted 27
September 2005; published online 23 November 2005
and change children’s and adults lives. One of the most
important and well-known global nutritional problems is
iodine deficiency, and its deficiency is the most common
preventable cause of mental disability in the world (IDD Key
Messages Generic Tool Kit 4). It is estimated that more than
one billion people, concentrated primarily in less-developed
countries, are unable to consume adequate levels of iodine.
Only during the last decade, it has been realized that IDDs
are the leading cause of intellectual impairment (Hetzel,
1993). Goiters are the most obvious sign of IDD.
Risk factors for goiter are those that do not seem to be a
direct cause of the disease, but seem to be associated in some
way. Having a risk factor for goiter makes the chances of
Risk factors of goiter
SM Mousavi et al
427
getting the condition higher, but does not always lead to
goiter. The risk factors for goiter include: iodine deficiency
(the most common), geographic regions with low iodine,
malnutrition, goiterogen such as turnips–kale–soya, poverty,
pregnancy and a low level of education. The involvement
of other factors (dietary or nondietary) besides iodine
deficiency might interact in the genesis of thyroid enlargement (Zali et al., 1994).
The IDD program begun 15 years ago in Iran, using iodized
salt with potassium iodated, and its coverage was sufficient
(urban 95% and rural 92%) in 2000. In the periodic
yearly medical examination of primary school girls in Qom
city of Iran, we found that the prevalence of goiter was 30%
in 2002. Why was the prevalence of simple goiter high in
this population, in spite of the sufficient iodized salt
coverage in this city, and after over 15 years past the IDD
program? The aim of the present study was to answer this
question and to examine the relations between demographic
variables, habits and socioeconomic factors for goiter in
these girls.
Materials and methods
Study design
Qom city is 120 km southwest of Tehran, the capital of
Iran, and its population is about 1 000 000. It is divided
into four district areas. This case-controlled study was
conducted from January to May 2002, according to Qom
city districts and the latest census of the number of girls
in primary schools, using multistage, proportional simple
random sampling. With the assumption of goiter prevalence
30%, a ¼ 0.05, d ¼ 0.05 and power 80%, we selected
and performed thyroid exams in 1050 girl students in
primary schools. All of them were clinically examined
for the presence of goiter. Examination of the thyroid
gland was made by inspection and palpation according
to the criteria endorsed by the World Health Organization
(WHO) and the International Council for The Control
of Iodine Deficiency Disorders (ICCIDD/UNICEF/WHO,
1990).
Classification of goiter is as follows:
GradeDescription
0
No goiter
IA
Thyroid lobes larger than ends of thumbs
IB
Thyroid enlarged, visible with head tilted back
II
Thyroid enlarged, visible with neck in normal position
III
Thyroid greatly enlarged, visible from about 10 m.
We found 284 cases of girls in primary schools who had
goiter by clinical exams with WHO classification. Of
students who had no goiter in clinical exam, we randomly
selected 288 students as a control group. We measured age,
weight, height in all cases and in the control group. Age,
weight and height of each student was compared with the
growth chart of weight per height and height per age, and
categorized into three groups: under percentile 3, between
percentile 3 and 97, and over percentile 97, for each student.
Then we interviewed the mothers of these students with a
simple data collection form.
Questionnaire (data collection form)
We used 24 closed questions to detect the demographic
variables, physical thyroid exams, goiterogen consumption,
type and amount of salt usage and its type of storage, family
socioeconomic situation (SES) (we classified the families into
three categories socioeconomically with regard to family
income, mother’s educational level, house situation, immigration and area of the city), and the nationality. We made
our questionnaire standard after interviewing 30 randomly
selected girls’ mothers from each group.
Statistical methods
We used SPSS 11.5 for Windows software to manage the
data and to perform descriptive and analytic statistical
tests. To examine the association of each factor with the
case and control groups, we used the Pearson w2 test, Fisher
exact test (two-sided) and Student’s t-test. Univariate logistic
regression analysis was performed to calculate OR with CI
95%. P-value o0.05 was considered statistically significant.
Then those factors were entered into a multinomial logistic
regression analysis, and the confounder’s effects were
measured.
Results
All students were females. The mean7s.d. ages of cases and
controls were 8.771.3 years (range 7–12 years) and 8.971.3
years (range 6–12 years), P-value was 0.022. There is a
statistically significant difference between cases and controls
with regard to age, but this statistical difference was seen due
to the high sample size, and it was not clinically significant
(mean age of cases and controls had 2.4 months difference),
but we measured its effect by multinomial logistic regression
analysis.
In Table 1, we showed the mean of weight and height of
cases and controls. As the mean of weight and height in the
Table 1
Subject baseline characteristics
Group
N
Mean
s.d.
s.e.m.
P-value
Weight
Case
Controlled
284
288
24.83
26.07
6.383
8.523
0.379
0.502
0.049
Height
Case
Controlled
284
288
127.40
129.99
9.088
10.326
0.539
0.608
0.002
European Journal of Clinical Nutrition
Risk factors of goiter
SM Mousavi et al
428
two groups showed a statistically significant difference, we
measured their effects by multinomial logistic regression
analysis.
The mean family number of cases and controls was
5.471.7 and 5.671.8, and there was no statistically
difference between them.
In the cases group, the frequency of grade I goiter was 236
(83.1%) and grade II was 48 (15.9%). We did not find any
grade III goiter in these students.
There were no significant differences between cases and
controls with regard to height/age percentile, history of kale,
turnip, soya, fish, iodine and salt consumption during the 1
month before, mean daily salt usage, mothers’ job, mothers’
education, family poverty, family SESs, immigration and
nationality. But we found a statistical significant difference
between cases and controls in the frequency of weight/
height percentile and also type of salt storage in the houses.
These associations and their ORs has been shown in Tables
2–4.
The results of linear regression analysis are shown in Table 3.
As it seems, only the type of storage of salt in the house is
significantly associated with goiter (P-value ¼ 0.002).
Table 2 Freqency of factors in case and control groups
Variables
Under percentile 3 of weight/height chart
Under percentile 3 of height/age chart
Kale consumption during 1 month ago
Turnip consumption during 1 month ago
Soya consumption during 1 month ago
Fish consumption during 1 month ago
Iodine salt consumption during 1 month ago
Storage of salt in opened container in the house
Under 10 g/day mean daily salt use
Employed mother of children
Uneducated mother of children
Povertya
Low socioeconomic situation
Resident under 10 years in Qom city
Foreign nationality
Case (%)
Control (%)
Pearson w2 P-value
13.7
3.2
67.3
68
43.7
79.6
98.9
72.9
3.2
6.7
20.1
81.7
36.3
20.4
6.3
21.5
3.5
70.8
64.4
45.5
74.3
99.3
61.1
5.2
6.3
24.7
78.1
44.4
18.8
3.5
0.014
0.840
0.354
0.393
0.661
0.135
0.642
0.003
0.224
0.831
0.189
0.287
0.873
0.614
0.112
Odd’s ratio (95% CI)
0.58
0.910
0.846
1.163
0.929
1.347
0.655
1.711
1.679
0.093
0.767
1.249
0.693
1.112
0.532
(0.37–0.90)
(0.364–2.274)
(0.593–1.206)
(0.822–1.646)
(0.668–1.292)
(0.911–1.993)
(0.109–3.950)
(1.202–2.435)
(0.722–3.901)
(0.477–1.811)
(0.517–1.139)
(0.829–1.883)
(0.612–1.518)
(0.736–1.681)
(0.241–1.173)
a
Poverty ¼ family income under 1 250 000 rials/month (equal to 144 US$/month) according to the Governmental definition for poverty in 2002.
P value o0.05 is significant.
Table 3 Risk factors of goiter derived from linear regression analysis
Unstandardized coefficients
(Constant)a
Age
Weight/height
Height/age
Kale consumption
Turnip consumption
Soya consumption
Fish consumption
Iodine salt consumption
Type of storage salt in the house
Mean daily salt consumption
Mother’s job
Mother’s education
Family income
House situation
Population density in the house
Socioeconomic situation
Time of residency in Qom city
Nationality
District of Qom City
a
Dependent variable: case controlled.
P value o0.05 is significant.
European Journal of Clinical Nutrition
Standardized coefficients
B
S.e.
b
0.615
0.027
0.097
0.116
0.054
0.026
0.004
0.042
0.040
0.158
0.091
0.032
0.012
0.095
0.023
0.046
0.090
0.027
0.133
0.044
0.520
0.016
0.053
0.106
0.049
0.047
0.044
0.057
0.226
0.051
0.105
0.095
0.025
0.053
0.051
0.048
0.066
0.054
0.101
0.025
0.075
0.078
0.046
0.050
0.025
0.004
0.036
0.007
0.149
0.037
0.016
0.030
0.138
0.022
0.046
0.127
0.021
0.057
0.094
t
1.182
1.672
1.837
1.095
1.112
0.554
0.092
0.742
0.176
3.117
0.863
0.334
0.492
1.791
0.457
0.958
1.365
0.500
1.315
1.742
Sig.
0.238
0.095
0.067
0.274
0.266
0.580
0.927
0.459
0.860
0.002
0.388
0.739
0.623
0.074
0.648
0.339
0.173
0.617
0.189
0.082
95% CI for B
Lower bound
Upper bound
1.637
0.005
0.201
0.092
0.150
0.066
0.082
0.069
0.404
0.058
0.116
0.155
0.062
0.009
0.123
0.048
0.040
0.079
0.331
0.006
0.407
0.059
0.007
0.325
0.041
0.118
0.090
0.154
0.483
0.258
0.298
0.218
0.037
0.198
0.077
0.140
0.221
0.133
0.065
0.093
Risk factors of goiter
SM Mousavi et al
429
Table 4 Risk factors of goiter derived from multinomial logistic regression
Number (%) a
Parameter
P-value
Cases (n ¼ 284)
Controls (n ¼ 288)
OR (95% CI)
Age group
6–9 years old
9–12 Years old
205 (72.2%)
79 (27.8%)
175 (60.8%)
113 (39.2%)
NA
NA
Weight/Height
o3 Percentile
Between 3 and 97 percentiles
497 percentile
39 (13.7%)
241 (84.9%)
4 (1.4%)
62 (21.5%)
223 (77.4%)
3 (1.0%)
0.335 (0.054–2.080)
0.541 (0.091–3.212)
1.00 (ref.)
Height/Age
o3 Percentile
Between 3 and 97 percentiles
497 Percentile
9 (3.2%)
275 (96.8%)
0 (0.0%)
10 (3.5%)
274 (95.1%)
4 (1.4%)
Kale consumption
Yes
No
191 (67.3%)
93 (32.7%)
204 (70.8%)
84 (29.2%)
0.724 (0.480–1.091)
1.00 (ref.)
0.123
Turnip consumption
Yes
No
193 (68.0%)
91 (32.0%)
186 (64.6%)
102 (35.4%)
1.210 (0.811–1.805)
1.00(ref.)
0.350
Soya consumption
Yes
No
124 (43.7%)
160 (56.3%)
131 (45.5%)
157 (54.5%)
0.935 (0.645–1.354)
1.00 (ref.)
0.720
Fish consumption
Yes
No
226 (79.6%)
58 (20.4%)
214 (74.3%)
74 (25.7%)
1.319 (0.811–2.147)
1.00 (ref.)
0.264
Iodine salt consumption
Yes
No
281 (98.9%)
3 (1.1%)
286 (99.3%)
2 (0.7%)
1.163 (0.170–7.950)
1.00 (ref.)
0.878
Type of salt storage in the house
Opened parcel
Closed parcel
207 (72.9%)
77 (27.1%)
176 (61.1%)
112 (38.9%)
2.201 (1.412–3.428)
1.00 (ref.)
0.000
Mean daily salt consumption
X10 g/day
o10 g/day
275 (96.8%)
9 (3.2%)
273 (94.8%)
15 (5.2%)
1.545 (0.630–3.784)
1.00 (ref.)
0.342
Mother’s job
Unemployed
Employed
265 (93.3%)
19 (6.7%)
270 (93.8%)
18 (6.3%)
1.141 (0.478–2.725)
1.00 (ref.)
0.767
0.625
0.684
0.780
0.735
1.00
(0.220–1.777)
(0.261–1.793)
(0.311–1.954)
(0.303–1.782)
(ref.)
0.378
0.440
0.596
0.496
Mother’s education
Illiterate
Primary
Secondary
Diploma
University degree
57
87
70
48
22
(20.1%)
(30.6%)
(24.6%)
(16.9%)
(7.7%)
71
91
63
44
19
(24.7%)
(31.6%)
(21.9%)
(15.3%)
(6.6%)
0.240
0.499
NA
NA
1.00 (ref.)
Family income
o600 000 rials/month
600 000–1 250 000 rials/month
41 250 000 rials/month
94 (33.1%)
138 (48.6%)
52 (18.3%)
106 (36.8%)
119 (41.3%)
63 (21.9%)
2.148 (0.862–5.349)
1.718 (0.875–3.374)
1.00 (ref.)
0.101
0.116
House situation
Rental
Ownership
92 (32.4%)
192 (67.6%)
94 (32.6%)
194 (67.4%)
0.978 (0.637–1.501)
1.00 (ref.)
0.918
Population density in the house
Commensurate
Not commensurate
144 (50.7%)
140 (49.3%)
130 (45.1%)
158 (54.9%)
1.190 (0.794–1.783)
1.00 (ref.)
0.401
European Journal of Clinical Nutrition
Risk factors of goiter
SM Mousavi et al
430
Table 4 Continued
Number (%) a
Parameter
P-value
Cases (n ¼ 284)
Controls (n ¼ 288)
OR (95% CI)
Socioeconomic situation
High
Medium
Low
43 (15.1%)
138 (48.6%)
103 (36.3%)
45 (15.6%)
115 (39.9%)
128 (44.4%)
2.415 (0.748–7.795)
2.099 (1.029–4.282)
1.00 (ref.)
0.140
0.041
Time of residency in Qom city
o10 Years
410 Years
58 (20.4%)
226 (79.6%)
54 (18.8%)
234 (81.3%)
1.079 (0.683–1.706)
1.00 (ref.)
0.743
Nationality
Iranian
Foreigner
266 (93.7%)
18 (6.3%)
278 (96.5%)
10 (3.5%)
0.471 (0.190–1.163)
1.00 (ref.)
0.103
District of Qom city
1.00
2.00
3.00
4.00
34
48
45
157
28
57
43
160
1.553
2.880
2.051
1.00
0.196
0.005
0.041
(12.0%)
(16.9%)
(15.8%)
(55.3%)
(9.7%)
(19.8%)
(14.9%)
(55.6%)
(0.797–3.027)
(1.376–6.027)
(1.032–4.078)
(ref.)
a
Unless otherwise stated. CI ¼ confidence interval; OR ¼ odds ratio.
Discussion and conclusion
In the present study, Pearson’s w2 test showed weight/height
OR: 0.58 (0.37–0.90), P-value ¼ 0.014, and type of salt
storage in the houses OR: 1.711 (1.202–2.435), P-value ¼
0.003 significantly associated with goiter, and from linear
regression analysis, which is shown in Table 3, it seems
that only the type of salt storage is significantly associated
with goiter (P-value ¼ 0.002). But, after measuring age,
weight and height as covariates, we analyzed multinomial
logistic regression to assess the association of parameters
with goiter and found the storage of iodized salt in open
containers, OR: 2.201 (1.412–3.428), P-value o0.0001,
medium SES, OR: 2.099 (1.029–4.282), P-value ¼ 0.041,
district 2 of Qom city OR: 2.880 (1.376–6.027), P-value ¼
0.005, and district 3 of Qom city OR: 2.051 (1.032–4.078),
P-value ¼ 0.041, to be the major risk factors for goiter in this
population.
Potassium iodated salt can be evaporated very easily, so the
iodized salt in an open container may be free of or have less
iodine. Unfortunately, we did not examine the content of
iodine of the salt in the salt stored in the households during
the study, and, after the analysis of data, we found these
differences between cases and controls with regard to salt
storage. Then we decided to examine the iodine content of
salt consumed in households, but because of summer
holidays the schools were closed, and most of the families
were out of the districts, and we were not able to examine it.
So our study has this limitation.
We also did not measure urinary iodine excretion. This
project needs a huge budget, which should be supported by
European Journal of Clinical Nutrition
health foundations. Of course, this project was performed as
medical students’ thesis and it was not under any funding
supports.
The first epidemiological study of IDD (Emami et al. (1969)
by the Institute of Nutrition) had shown that iodine
deficiency was endemic in many areas in Iran. After that,
many studies suggested that iodine deficiency is endemic in
Iran, and that it is more prevalent in female than in male
subjects (Navaei et al., 1986; Sheikholeslam and Azizi, 1992;
Sheikholeslam and Sadvandian, 1993; Zahedi et al., 1995;
Rajabian et al., 1996; Deshad et al., 1998; Azizi et al., 2001a;
Iran Epidemiological Data – Iodine). According to the WHO,
a total goiter rate of 5% or more in primary school children
(6–12 years) should signal the presence of a public health
problem (World Health Organization Document, 1994). The
IDD program had begun 15 years ago in Iran using iodized
salt with potassium iodated. Many studies showed that the
prevalence of goiter had decreased in Iran during this period
(IDD News letter, 1996; Azizi et al., 2001b; Ravanshad et al.,
2003). In 1996 the coverage of iodized salt usage was 50%,
but in 2000 its coverage was sufficient (urban 95% and rural
92%). In spite of this sufficiency, the prevalence of goiter was
reported to be 32.1% in the same year (Noorbala et al., 2000)!
Many studies evaluated the IDD program and its effect on
thyroid function by urinary iodine excretion measurements
in Iran (Azizi et al., 2001c, 2005; Mirmiran et al., 2003;
Salarkia et al., 2003; Aminorroaya et al., 2004). Azizi et al.
(2001b), who surveyed in each of the 26 provinces of Iran,
according to WHO classification and urinary iodine excretion, found that goiter was endemic in all provinces, but the
majority had a small (grade 1) goiter. Median urinary iodine
Risk factors of goiter
SM Mousavi et al
431
was 20.5 mg/dl. In all, 85% had urinary iodine greater than
10 mg/dl. In all 26 provinces, the median urinary iodine was
above 13 mg/dl, 6–9% of the school children had urinary
iodine less than 5 mg/dl. No significant differences were
observed between boys and girls, or rural and urban
residents, with respect to urinary iodine excretion. It was
seen that, 7 years after beginning salt iodization and 2 years
after compulsory iodization of table salt, urinary iodine
excretion had reached adequate levels in school children.
Considering the percentage of households consuming
iodized salt and that the IDD program is well followed, they
concluded that iodine deficiency had been controlled in
Iran.
The results of this study have shown that the use of iodized
salt caused an increase in excreted urinary iodine and a
decrease in the prevalence of thyroid goiter, especially in
younger age groups. Consumption of iodized salt with 40
parts per million (p.p.m.) iodine had not caused increased
prevalence of thyroid dysfunction in this area. The benefits
of iodized oil administration in decreasing goiter size and in
resuming normal thyroid function up to 3 years after the
intervention have been shown in a study (Mirmiran et al.,
2002).
High coverage of iodized salt does not seem to overcome
goiter in Iran as much as would be expected, despite the lack
of any apparent impact of the potential goitrogenic foods.
Could there be other goitrogenic factors involved on a large
scale? Unfortunately, there are few articles about the risk
factors of goiter in Iran.
In 1997, 8000 male and female 6–18-year-old students
were selected by cluster sampling in schools of Isfahan. Their
thyroids were examined by four endocrinologists, and goiter
was staged on the basis of the WHO classification. As an
index of iodine consumption, urinary iodine concentrations
were measured in 3000 students. Goiter was observed in
62% of the students. Of the overall study group, 94% had
sufficient iodine consumption (urinary iodine concentration
of 10.0 mg/dl or more). Of those students who had sufficient
iodine intake, 63.2% had goiter. Despite sufficient iodine
intake, the prevalence of goiter was still high in Isfahan City.
Apparently, either this high prevalence has no relationship
to iodine deficiency and possibly other unknown goitrogens
are involved in the pathogenesis of goiter in Isfahan, or the
period of iodine intake had been too brief to affect thyroid
sizes. Inasmuch as goiter prevalence was also high in the
6–10-year-old children, who had iodized salt available for
most of their lives, the second option was less probable.
Another possibility was an increased rate of autoimmune
thyroid diseases (because of iodine repletion) that resembled
goiter during their early stages (Aminorroaya et al., 2001).
In our study, we found that the moderate SES of families
and their residence in districts 2 and 3 of Qom city might be
a risk factor for goiter. We should explain that districts 2 and
3 of Qom city are in the low to medium SES. Therefore, the
low to medium SES might be a risk factor for goiter, and also
something else about living in districts 2 or 3 might lead to
an increased risk of goiter, such as water supplies and cultural
differences, which need to be confirmed by other studies.
There may be another suggestion about this finding, in
which medium SES results in higher goiter rates rather than
low rates; high SES is associated with an even higher rate, but
this is not significant, presumably because the sample size
for that group is low.
According to a food consumption survey in Shahryar town
near Tehran, an endemic area near the capital city of Iran in
1990, significant reverse correlations were found between
goiter prevalence and vitamin A and protein intakes, and
they concluded that iodine deficiency played a key role in
goiter. That study explained the need for further consideration about the association of other dietary factors (Kimiagar
et al., 1990).
Janghah (1997) and Ghamie (1997) reported that 8.66% of
a subsample of 6–11-year-old school girls in Shiraz were
iodine deficient according to urinary iodine/creatinine ratio.
On the other hand, Ravanshad et al. (2003) revealed that 4.7
and 12.1% of a subsample of girls according to two indices,
that is, urinary iodide excretion and urinary iodide/creatinine ratio, respectively, were iodine deficient and prevalence
of goiter was 25% in Shiraz. Could there be iron deficiency
involved in it? Azizi et al. (2002) suggested that iron
deficiency was associated with a high prevalence of goiter
in Iranian schoolchildren. According to this study, because
iron deficiency may impair the efficacy of iodine supplementation, they determined the relation between serum
ferritin and goiter, urinary iodine and thyroid hormones
following iodized salt supplementation. Total goiter rates
were 80 and 20% in children with ferritin concentrations
o10 mg/dl and X10 mg/dl, respectively (Po0.001). Increased serum T3 and decreased resin T3 uptake was present
in those with lower serum ferritin levels; however, free
T3 and T4 index, serum T4 and TSH were not significantly
different between those with low and normal ferritin. Yavuz
et al. (2004) evaluated the effect of iron status on thyroid
hormone profile in adolescents living in a mildly iodinedeficient area in Turkey, and found that thyroid hormone
levels of the children with anemia were not significantly
different compared to children without anemia. No significant correlation was found between thyroid hormones and
iron status. Zimmermann et al. (2002) studied to determine if
cofortification of iodized salt with Fe would improve the
efficacy of iodine in goitrous children with a high prevalence
of anemia. In a 9-month, randomized, double-blind trial,
6–15-year-old children (n ¼ 377) were given iodized salt
(25 mg iodine/g salt) or dual-fortified salt with iodine (25 mg
iodine/g salt) and Fe (1 mg Fe/g salt, as ferrous sulfate
microencapsulated with partially hydrogenated vegetable
oil). They concluded that the addition of encapsulated Fe to
the iodized salt improved the efficacy of iodine in goitrous
children with a high prevalence of anemia. Hess et al. (2002)
determined whether iron supplementation in goitrous,
iron-deficient children would improve their response to
iodized salt. They conducted a randomized, double-blind,
European Journal of Clinical Nutrition
Risk factors of goiter
SM Mousavi et al
432
placebo-controlled trial in 5–14-year-old children in the
Ivory Coast. They concluded that iron supplementation
improved the efficacy of iodized salt in goitrous children
with iron deficiency.
There may be other goitrogenic factors involved in a
goiter, such as the selenium concentration; Nouarie et al.
(2004) found that the median serum selenium concentrations were very different in four provinces of Iran. Raie
(1996) compared the levels of Hg, As and Se in hair samples
from Iran and Glasgow, and revealed significantly lower
levels of these trace elements in samples conducted from
Iran; it may be that most Iranian soils contain relatively
low concentrations of the Se. Aydin et al. (2002) conducted a
study to establish the effects of iodine and selenium levels
on thyroid gland size and thyroid function in 73 healthy
schoolchildren, 7–12 years old, living in an endemic goiter
area in Turkey. They found that thyroid volumes of the
children were negatively correlated with serum selenium
levels, but there was no correlation with urinary iodine levels
and thyroid hormones, and concluded that schoolchildren
in this area had significant goiter problems, probably due to
iodine and selenium deficiencies.
The main finding of our study is that iodized salt storage in
an open container may be a risk factor for goiter. Iodine
stability and iodine losses in iodized salt following different
storage methods had been evaluated by many studies in the
world. Taga et al. (2004) studied five groups of salt samples
from three provinces of Cameroon. Each group included a
specimen from the factory, wholesalers, retailers and households. Iodine content was measured by the volumetric
method. The results showed that the iodine levels in salt
decreased substantially between the factory and the consumer; percentages of iodine loss in these samples varied
from 44.8 to 82.3%. Iodine levels were highest in finegrained salt. Iodine concentration also decreases after
storage, perhaps as a function of the type and duration of
storage, temperature, the packaging material and presence
of impurities in salt. This study shows that even salt with an
initial high iodine concentration may reach consumers
with insufficient levels for daily needs. A survey of 180 rural
families from different zones of Haryana State was carried
out by Punia et al. (2002) to find out the type of salt used and
intake, and the domestic storage practices. Analysis of iodine
in salt samples showed that, of samples from three zones,
39% contained no iodine; 9% had o15 p.p.m., 14% had 15–
29 p.p.m. and 37% had X30 p.p.m. The results indicated that
most of the people in rural Haryana consumed powdered salt
and stored it in airtight containers. Biber et al. (2002) had
shown that, after the salt was stored at room temperature
with a relative humidity of 30–45% and in sealed paper bags
for 3 years, 58.5% of iodine content was lost in approximately 3.5 years. According to a survey that was conducted
on a random sample of 400 households in the Marcory
district of Abidjan by Adou et al. (2002), they observed that
in 23.3% of households the iodine content of salt was weak
(o30 p.p.m.). Contents higher than the upper limit of
European Journal of Clinical Nutrition
normality (30–50 p.p.m.) were found in 44.8% of cases. The
level of iodine was adequate for 32% of households.
As the coverage of iodine salt is over 95% in Iran, we advise
health policymakers and other decision makers, and investigators in Iran, to design high-quality studies to measure
potential goitrogenic factors and the effect of different
storage methods of iodized salt on iodine losses. Investigators should not restrict their outcomes to goiter rates and
urinary iodine excretion, but should include other outcome
measures such as mental and physical development in
children, mortality and others. We also recommend the
study of consumers’ behavior regarding the purchase and
storage of salt, and the determination of the iodine content
of dietary salt in Iran.
As a main practical comment, we advise mass education
about iodized salt storage in closed containers for families.
As many studies showed the effect of packaging and
storage of iodized salt on iodine losses, if it has been studied
adequately, we recommend meta-analysis studies to confirm
the results and we think that there needs to be increased
international attention with regard to this issue. If others
come up with similar conclusions, then increased international attention on this aspect is needed. The IDD
program needs to revise and focus on the risk factors of
goiter, method of packaging and storage of iodized salt, and
investigators should not restrict their outcomes to goiter
rates and urinary iodine excretion, but should include other
outcome measures such as mental and physical development
in children, mortality and others. Investigators should pay
special attention to adverse effects and their report in
primary studies, and should assess children (including very
young children who may have a relatively low salt
consumption) separately from adults.
However, we do not know if there is any other factor
that could be the cause of goiter in this population, such
as iron deficiency, selenium deficiency, autoimmunity or
tumors. So we recommend the study of these factors in
this population and the other risk factors of goiter in the
different geographical areas of Iran because of the differences
in the socioeconomics factors, cultural and nutritional
habits.
Acknowledgements
This study had been supported by permission letters for
our activities (not funding support) from Qom Health
Network and Medical Services, Qom Medical University
and Qom Primary School Education Office, Fathemieh
Medical University. We wish to thank the anonymous
reviewers of the journal for their helpful comments on
previous versions of the manuscript, and Ms Zinat Sadat
Mousavi for her comments on correcting the English text of
this article, Ms Somayeh Asbaghi Namini for the kind
attention and many practical comments about the nutrition
items of the article.
Risk factors of goiter
SM Mousavi et al
433
References
Adou P, Aka D, Ake M, Koffi M, Tebi A, Diarra-Nama AJ (2002).
Assessment of iodine content of dietary salt in Abidjan (Cote
d’Ivoire) Sante 12, 18–21.
Aminorroaya A, Amini M, Rezvanian H, Kachoie A, Sadri G,
Mirdamadi M et al. (2001). Effects of iodized salt consumption
on goiter prevalence in Isfahan: the possible role of goitrogens.
Endocr Pract 7, 95–98.
Aminorroaya A, Rohani S, Sattari G, Haghighi S, Amini M (2004).
Iodine repletion, thyrotoxicosis and atrial fibrillation in Isfahan,
Iran. Ann Saudi Med 24, 13–17.
Aydin K, Kendirci M, Kurtoglu S, Karakucuk EI, Kiris A (2002). Iodine
and selenium deficiency in school-children in an endemic goiter
area in Turkey. J Pediatr Endocrinol Metab 15, 1027–1031.
Azizi F, Hedayati M, Rahmani M, Sheikholeslam R, Allahverdian S,
Salarkia N (2005). Reappraisal of the risk of iodine-induced
hyperthyroidism: an epidemiological population survey. J Endocrinol Invest 28, 23–29.
Azizi F, Mirmiran P, Sheikholeslam R, Hedayati M, Rastmanesh R
(2002). The relation between serum ferritin and goiter, urinary
iodine and thyroid hormone concentration. Int J Vitam Nutr Res
72, 296–299.
Azizi F, Navai L, Fattahi F (2002). Goiter prevalence, urinary iodine
excretion, thyroid function and anti-thyroid function and antithyroid antibodies after 12 years of salt iodization in Shahriar,
Iran. Int J Vitam Nutr Res 72, 291–295.
Azizi F, Rahmani M, Allahverdian S, Hedayati M (2001a). Effects of
salted food consumption on urinary iodine and thyroid function
tests in two provinces in the Islamic Republic of Iran. East Mediterr
Health J 7, 115–120.
Azizi F, Shaikholeslam R, Hedayati M, Mirmiran P (2001b). Goiter
and urinary iodine in Iranian school children. Teb-va-Tazkiyeh 40,
44–51.
Azizi F, Sheikholeslam R, Hedayati M, Mirmiran P (2001c). Monitoring of goiter and urinary iodine in primary students of Lorestan
province. Lorestan Univ Health Med J 8, 49–53.
Biber FZ, Unak P, Yurt F (2002). Stability of iodine content in iodized
salt. Isotopes Environ Health Stud 38, 87–93.
Deshad H, Satari M, Monsef A (1998). Thyroid single nodule in
Hamadan province. Sci J Hamadan Univ 11, 5–9.
Emami A, Shahbazi H, Sbzevari M et al. (1969). Goiter in Iran. Am J
Clin Nutr 22, 1584.
Ghamie S (1997). Prevalence study of goiter in 11–14 years old school
girls in Shiraz, Iran. MS Thesis, School of Medicine, Shiraz
University of Medical Sciences (unpublished data).
Hess SY, Zimmermann MB, Adou P, Torresani T, Hurrell RF (2002).
Treatment of iron deficiency in goitrous children improves
the efficacy of iodized salt in Cote d’Ivoire. Am J Clin Nutr 75,
743–748.
Hetzel BS (1993). The control of iodine deficiency. Am J Public Health
83, 494–495.
ICCIDD/UNICEF/WHO (1990). A Practical Guide to the Correction of
Iodine Deficiency. Manual No. 3.
IDD Key Messages Generic Tool Kit 4. http://www.tulane.edu/Bicec/
iddcommguidetk4.htm.
IDD News letter (1996) Vol. 12, No. 4, November.http://www.people.
virginia.edu/Bjtd/iccidd/newsletter/idd1196.htm.
Iran Epidemiological Data – Iodine. http://www.tulane.edu/Binternut/
Countries/Iran/iraniodine.html.
Janghah A (1997). Prevalence study of IDD among primary school
girls in Shiraz, Iran. Pediatric Thesis (Persian), School of Medicine,
Shiraz University of Medical Sciences (unpublished data).
Kimiagar M, Azizi F, Navai L, Yassai M, Nafarabadi T (1990). Survey of
iodine deficiency in a rural area near Tehran: association of food
intake and endemic goitre. Eur J Clin Nutr 44, 17–22.
Mirmiran P, Hajipour R, Azizi F (2003). Iodized salt consumption
maintains euthyroidism in iodine-deficient hypothyroid subjects.
Int J Vitam Nutr Res 73, 187–191.
Mirmiran P, Kimiagar M, Azizi F (2002). Three-year survey of effects
of iodized oil injection in schoolchildren with iodine deficiency
disorders. Exp Clin Endocrinol Diabetes 110, 393–397.
Navaei L, Kimiagar M, Azizi F (1986). Epidemiology of goiter in
Shahriyar. Med J Shaheed Beheshti Univ Health Med Serv 10, 8–11.
Noorbala A, Mohammad K, Malekafzali H, Majdzadeh SR, Karimloo
M, Mirjafari Firoozabadi SJ et al. (2000). Health and Disease Survey
in Iran. Ministry of Health, National Medical Research Center:
Iran, pp 104–105.
Nouarie M, Pourshams A, Kamangar F, Sotoudeh M, Derakhshan MH,
Akbari MR et al. (2004). Ecologic study of serum selenium and
upper gastrointestinal cancers in Iran. World J Gastroenterol 10,
2544–2546.
Punia D, Yadav SK, Gupta M, Khetarpaul N (2002). Note: storage
practices, salt intake and iodine content of salt consumed in
rural households of Haryana State, North India. Nutr Health 16,
337–342.
Rajabian R, Abdinegad A, Praizadeh J, Shahbazi H, Sayadpoor K,
Abdolsalami HR (1996). IDD in Mashhad and Neishboor. Iran J
Med Assoc 15, 25–30.
Raie RM (1996). Regional variation in As, Cu, Hg, and Se and
interaction between them. Ecotoxicol Environ Saf 35, 248–252.
Ravanshad Sh, Setoudeh Maram E, Nader F, Mostafavy H (2003).
Prevalence study of iodine deficiency disorders among high school
girls in Shiraz, Islamic Republic of Iran, 1996–1997. Pak J Med Sci
19, 70–74.
Salarkia N, Hedayati M, Mirmiran P, Kimiagar M, Azizi F (2003).
Evaluation of the impact of an iodine supplementation programme on severely iodine-deficient schoolchildren with hypothyroidism. Public Health Nutr 6, 529–533.
Sheikholeslam R, Azizi F (1992). Prevention of iodine deficiency
disorders. A report about IDD activities in Iran. Daroo Darman J 9,
29–32.
Sheikholeslam R, Sadvandian S (1993). Iodine Deficiency Disorders for
Health Worker Education. Nutrition, Health and Family Planning
Office, Ministry of Health and Medical Education: Iran, pp 36–37.
Taga I, Massouke DD, Ndomou M, Yonkeu JN (2004). Iodized salt in
Cameroon. Sante 14, 161–165.
World Health Organization Document (1994). Indictors for Assessing
Iodine Deficiency Disorders and Their Control Through Salt Iodization.
World Health Organization: Geneva. (document no. WHO/NUT/
94.6).
Yavuz O, Yavuz T, Kahraman C, Yesildal N, Bundak R (2004). The
relationship between iron status and thyroid hormones in
adolescents living in an iodine deficient area. J Pediatr Endocrinol
Metab 17, 1443–1449.
Zahedi AS, Saboor H, Poorseraj S (1995). A hyper endemic region for
goiter in Khozestan province. Med J Shaheed Beheshti Univ Health
Med Serv 19, 35–41.
Zali MR, Mohammad K, Azam K, Masgedi MR (1994). Thyroid
situation in Iran according to Health and Disease Survey – 1990.
Iranian J Med Assoc 13, 113–122.
Zimmermann MB, Zeder C, Chaouki N, Torresani T, Saad A, Hurrell
RF (2002). Addition of microencapsulated iron to iodized salt
improves the efficacy of iodine in goitrous, iron-deficient
children: a randomized, double-blind, controlled trial. Eur J
Endocrinol 147, 747–753.
European Journal of Clinical Nutrition