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Original Studies |
Department of Endocrinology (F.A.-L., L.A., E.M., P.V., D.M., F.L., T.R., L.G., R.V., A.P.), University of Pisa, Pisa; and the Department of Internal Medical Sciences, University of Cagliari (A.B.), Cagliari, Italy
Address all correspondence and requests for reprints to: Fabrizio Aghini-Lombardi, M.D., Department of Endocrinology, University of Pisa, via Paradisa 2, I-56124 Pisa, Italy.
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Abstract |
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Introduction |
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In the present study, the prevalence of thyroid disorders has been investigated in virtually the entire child population and in a high and representative proportion of the adult population living in Pescopagano, a southern Italian village with mild to moderate iodine deficiency.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The survey was conducted in Pescopagano, a southern Italian village located in the Lucan Apennines at 954 meters above the sea level. The nearest town is 70 km away. Pescopagano was selected for its long term exposure to iodine deficiency with no previous iodine prophylaxis. The economy of this area is progressively converting from agriculture to service activities. The usual diet consists mainly of local products. At the time of the survey, the registered population of Pescopagano was 2348 people. Daily commuters with neighboring towns accounted for 620 people. They were excluded from the survey because of their exposure to higher iodine dietary intake. A total of 317 people of the 1728 permanently residing in the village failed to respond to 2 consecutive calls to participate in the survey. Thus, 1411 residents were actually examined: 419 (215 males and 204 females) 1- to 14-yr-old children, representing 94.1% of this age group, and 992 (573 females and 419 males) of the 1368 subjects aged 15 yr or more, representing 72.5% of this age group and referred to as the adult population. General practitioners of the village actively took part in each step of the survey. Civil and health authorities strongly supported the project, and informed consent was obtained from parents of the minors and from adult subjects. A questionnaire sheet was completed for each subject and included personal and family histories of thyroid disease with details of treatment and special attention being paid to L-T4 and any other medication affecting thyroid function. Alimentary habits and coexistent autoimmune disorders were also taken into account. In the schoolchildren, population height and weight were measured.
A randomized sample of 75 adult subjects, drawn from the group of 317 subjects who failed to respond to the first and second calls, was personally approached by family physicians and invited to participate in the survey again. In 64 subjects complying with such personalized invitation, urinary iodine excretion (UIE) measurements and goiter assessments were performed. The data were compared with those obtained in the general survey.
UIE
Casual urinary samples were collected for measurement of iodine concentration by a colorimetric method using an autoanalyzer apparatus (Technicon, Rome, Italy) (10). The results were calculated as micrograms of iodine per L urine and are expressed as a median.
Thyroid ultrasound
Thyroid ultrasound examination was performed by a portable real-time instrument (Esaote, Biomedica, Firenze, Italy) using a 7.5-MHz linear transducer. Subjects were examined in the supine position with the neck hyperextended. Thyroid volume was calculated according to the formula of the ellipsoid model: width x length x thickness x 0.52 for each lobe (11). As previously described, goiter as assessed by ultrasound was defined when the thyroid volume was more than 2 SD above the mean thyroid volume of age-matched controls in children and of sex-matched controls in adults. The normal thyroid volume in children was obtained from 2709 children residing in urban nonendemic areas (12). The normal thyroid volume in adults residing in nonendemic areas and with no clinical or laboratory evidence of thyroid disease was 11.3 ± 6.8 mL (mean ± 2 SD) in males (n = 125) and 8.6 ± 4.4 mL in females (n = 132). Thus, in adults, thyroid volumes greater than 18.1 mL in males and 13 mL in females were considered to indicate goiter. The reproducibility of thyroid volume measurement by ultrasound was assessed by determining the interobserver error among 4 examiners in 30 children and 30 adults.
Thyroid function tests
Serum free T4 (FT4) and serum free T3 (FT3) were measured by RIA (FT4 Liso-Phase kit and FT3 Liso-Phase kit, Technogenetics, Milan, Italy). Serum TSH was measured by a sensitive immunoradiometric assay (Gamma Coat 125I, Incstar Corp., Stillwater, MN). The functional sensitivity of the TSH assay was 0.03 mU/L. The normal range, determined in 123 15- to 75-yr-old subjects, was 0.4–3.7 mU/L. Serum autoantibodies to thyroglobulin (TgAb) and thyroperoxidase (TPOAb) were measured by agglutination (Serodia-ATG and Serodia-AMC, Fujirebio, Inc., Tokyo, Japan).
Fine needle aspiration
Fine needle aspiration (FNA) was advised in all subjects with nodular goiter and was performed in 132 of 171 (77.2%) subjects who gave their consents. FNA was performed in 119 solid and mixed nodules larger than 1.5 cm. Smaller nodules were examined by FNA (n = 13) only when clinical findings or the echographic pattern suggested the opportunity of excluding malignancy.
Statistics
Statistical evaluation was performed by the 
2
test and t test using the Statxact Program of Cytel Software
Corp. (Cambridge, MA).
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Results |
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At the time of the survey, no subject was receiving treatment. Previous treatment with methimazole was documented in 9 patients with a past history of toxic nodular goiter. Six of 10 patients who were previously subjected to partial thyroidectomy and 11 subjects with nontoxic nodular goiter were receiving replacement therapy with L-T4. They all had normal serum concentrations of FT4, FT3, and TSH. No subject reported the use of iodized salt or iodine-containing drugs.
UIE
The median UIE was 55 µg/L (mean ± SD, 76
± 53). Values lower than 100 µg/L were found in 81% of subjects,
and values greater than 200 µg/L were documented in less than 1.0%
of subjects (Fig. 1
).
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As reported in Table 1, the overall
prevalence of goiter progressively increased with age. Thyroid
enlargement was found in 67 of 419 children (16.0%). The prevalence of
goiter progressively increased from 10.1% in 6- to 8-yr-old children
to 17.0% and 37.6% in 9- to 11-yr-old and 12- to 14-yr-old groups,
respectively. No thyroid abnormality was documented in children under 6
yr of age. All goitrous children had a diffuse goiter less than twice
the thyroid volume of age-matched controls, with the exception of one
14-yr-old girl and one 13-yr-old boy who had nodular goiter. No
significant difference was found in the prevalence of goiter between
females and males [39 of 204 (19.1%) and 28 of 215 (13.0%),
respectively].
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15 yr-old), goiter, regardless of thyroid
function, was observed in 583 of 992 subjects (58.8%). Ten patients
were previously subjected to partial thyroidectomy for nontoxic goiter.
Thus, the overall prevalence of goiter in the adult population was
59.8%. The prevalence of nodular goiter was negligible in the 15–25
yr age class, increased up to 28.5% in the 56–65 yr age class, and
declined in older subjects. The prevalence of goiter was not different
between females (59.5%) and males (58.0%). Among subjects with
enlarged thyroid (excluding patients previously subjected to
thyroidectomy), moderate goiter (
30 mL) was found in 62.3% of
subjects, large goiter (30–60 mL) was found in 30.2% of subjects, and
very large goiter (60 mL) was found in 7.5% of subjects. Symptoms
and/or signs indicating a compression of adjacent structures of the
neck were present in 142 goitrous subjects (14.3% of the adults). The
frequency of symptoms was related to thyroid size, being present in
5.2% of subjects with moderate goiter, in 46.6% of subjects with
large goiter, and in 93.2% of subjects with very large goiter.
Seventy-three subjects were considered possible candidates for surgery.
Surgical removal of the goiter because of severe pressure symptoms was
advised in 27 and has been performed in 6 subjects to date. Nontoxic goiter accounted for virtually all cases of goiter in children (64 of 67) and for the large majority of adults (490 of 593, 82.6%). Thyroid disorders associated with thyroid enlargement in the remaining subjects are described below.
Functional autonomy
For the purpose of the present study, thyroid functional autonomy
was defined by the finding of normal serum concentrations of
FT4 and FT3 and subnormal
serum TSH concentrations (<0.4 mU/L). Thyroid hormone medication and
other conditions leading to TSH suppression were excluded. As reported
in Table 2, thyroid functional autonomy
was found in 67 of 1411 (4.7%) subjects, with no difference between
females (5.2%) and males (4.1%). Its frequency progressively
increased with age from 0.7% in children to 15.4% in elderly subjects
(>75 yr old); the overall prevalence in the adult population was
6.4%. Thyroid functional autonomy was unrelated to goiter size and
occurred in both nodular (n = 36) and diffuse goiter (n =
31), but its relative frequency was significantly greater in the former
group (21.2% vs. 6.4%; P < 0.0001).
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Nine patients had a history of toxic nodular goiter. Active
hyperthyroidism was documented in 20 adults and in none of the 419
children. The overall prevalence of hyperthyroidism was 29 of 992
(2.9%) adults (Table 3), with no
difference between females (17 of 573, 2.96%) and males (12 of 419,
2.86%). Nine patients (0.9%) had toxic diffuse goiter, and 20 (2.0%)
had toxic nodular goiter, including 1 male with active toxic adenoma in
whom the diagnosis was confirmed by scintiscan and all 9 patients with
a past history of hyperthyroidism. Thus, the nonautoimmune/autoimmune
hyperthyroidism ratio was 2.2:1. Toxic diffuse goiter was equally
distributed in each class of adult age, whereas toxic nodular goiter
increased from 1.0% in 26–35 yr age class to 7.7% in the 56–65 yr
age class. No cases of toxic nodular goiter were found beyond the age
of 75 yr.
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No subject had previously been diagnosed and treated for hypothyroidism. Spontaneous overt hypothyroidism was newly diagnosed in 2 of 992 (0.2%) adults and in none of the 419 children. Both hypothyroid subjects were females (2 of 573, 0.34%) and had high serum TgAb and TPOAb titers. One of them had a reduced thyroid volume and diffuse hypoechogenicity at ultrasound, indicative of atrophic autoimmune thyroiditis, whereas the other had a diffuse goiter.
Subclinical hypothyroidism, as defined by serum TSH greater than 3.7
mU/L with serum levels of free thyroid hormones within the normal
range, was found in 38 of 992 (3.8%) adults with no difference between
females (25 of 573, 4.4%) and males (13 of 419, 3.1%). Ten of 38
subjects had humoral evidence (TPOAb and/or TgAb, 1:100) of thyroid
autoimmunity.
Serum thyroid antibodies and diffuse autoimmune thyroiditis
Figure 2 shows the prevalence of
thyroid autoantibody-positive tests (1:100 for both TPOAb and TgAb)
in each age class regardless of other thyroid abnormalities. The
overall prevalence was 12.6% (females, 17.3%; males, 7.0%) and
progressively increased from 2.4% in children to 21.9% in the 46–55
yr age class, with little change in older subjects. Thyroid
autoantibodies were more frequently found in goitrous (95 of 651,
14.6%) than in nongoitrous (45 of 760, 5.9%) subjects
(P < 0.0001).
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1:400) and thyroid echographic pattern of
diffuse hypoechogenicity indicative of diffuse autoimmune thyroiditis
(13) were found in 50 of 1411 (3.5%) subjects (Table 4): 44 were euthyroid, 5 were
subclinically hypothyroid, and 1 had overt hypothyroidism. Goiter was
present in 26 of these 50 subjects.
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As shown in Fig. 3, median TSH
values progressively decreased from 2.2 mU/L in children to 0.9 mU/L in
56- to 65-yr-old subjects, with no further changes in the older age
classes. No significant difference between males and females was found
in any age class. The mean serum TSH concentration in the adult
population was significantly lower (P < 0.0001) in
goitrous (1.4 ± 1.1 mU/L) than in nongoitrous (2.0 ± 2.4
mU/L) subjects.
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No subject with a past history of thyroid cancer was found. Of the 132 patients submitted to FNA, 1 had papillary thyroid cancer confirmed by histology. Thus, the prevalence of ascertained thyroid cancer in the study population was 1 of 1411. A follicular adenoma was documented by histology in an additional subject with a microfollicular pattern with nuclear atypias by cytology. Benign thyroid lesions at cytology were found in 116 (87.9%) subjects, whereas the FNA specimens were nondiagnostic in 14 (10.6%) subjects.
Other thyroid disorders
In a 53-yr-old male, clinical features of panhypopituitarism associated with low serum FT4, FT3, and TSH concentrations were documented, indicating the diagnosis of central hypothyroidism. Two cases of thyroid hemiagenesis with normal thyroid function were also identified.
Validation study
In the randomized sample, the median UIE was 51 µg/L, and the overall frequency of goiter was 54.7%, with no significant difference with respect to the study population.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The prevalence of goiter progressively increased with age, being 16.0% in children and 59.8% in adults. Age and sex goiter distributions were similar to those observed in other iodine-deficient areas (5, 6, 7, 8, 9, 14, 15, 16), but differed from those observed in iodine-sufficient areas in which the goiter prevalence is higher in young adults than in middle-aged and elderly people and is much more frequent in females than in males (2). Thus, it would appear that iodine deficiency not only overcomes the increased female susceptibility to develop goiter, but also influences the natural history of goiter by counteracting its declining prevalence with age. Rather than an increase, we observed a fall in goiter prevalence in very old subjects (>75 yr old), as reported in other iodine-deficient areas (5, 6, 7, 8, 9). The question of whether and to what extent this decline is due to the selection of people reaching such an advanced age remains to be established. On the basis of the UIE of 55 µg/L, Pescopagano could be classified as an area with mild to moderate iodine deficiency. Compared with areas with similar degrees of iodine deficiency, the prevalence of goiter observed in the present study appears to be much higher than expected, especially in the adults. This may be related to a prolonged exposure of this area to a more severe iodine deficiency in the past. As previously reported from other areas of Italy, silent prophylaxis due to improved socioeconomic and nutritional conditions most likely occurred in recent years, resulting in an improved iodine intake. This prevented the development of new goiters in younger subjects, but was not accompanied by a parallel reduction in the prevalence of established goiter (17).
In the present survey, thyroid nodularity was exceptional in children and was rare in 15- to 25-yr-old subjects, progressively increased with age up to 65 yr and tended to decline thereafter. Clinically significant pressure symptoms were not rare in the adults; 73 patients required medical attention for pressure symptoms, and surgery was advised in 27 subjects. These findings underscore the role of prolonged exposure to iodine deficiency in the growth of goiter and the progression of nodularity. The prevalence of thyroid nodularity in the adults living in Pescopagano was apparently lower than that recently reported from some iodine-sufficient areas using thyroid ultrasound (18, 19). The use of different criteria for the definition of nodularity largely accounts for this discrepancy. Although only lesions greater than 10 mm were considered in the present survey, lesions as small as 3–10 mm were included in the above reports.
The overall prevalence of overt hyperthyroidism was twice as high as that found in the Whickham survey (1, 3). At variance with iodine-sufficient areas, in which hyperthyroidism is mainly due to toxic diffuse goiter (4, 20, 21, 22, 23, 24), toxic nodular goiter accounted for the majority of thyrotoxic subjects living in Pescopagano, being twice as frequent as toxic diffuse goiter. Toxic nodular goiter occurred in older subjects and was more prevalent in males than in females. On the contrary, toxic diffuse goiter was equally distributed in different age classes of adults, with a pronounced preponderance of female subjects. The prevalence of thyroid functional autonomy progressively increased from 0.7% in children to 15.4% in subjects more than 75 yr old and was more frequent in subjects with nodular goiter. The prevalence of functional autonomy observed in the adults (6.4%) was much higher than that reported in iodine-sufficient areas, where this condition is rare (25, 26, 27, 28). When data from the survey carried out in the iodine-sufficient Whickham community were recalculated (3) using the same criteria adopted in this study, a frequency of 0.6% for functional autonomy was found.
Overt hypothyroidism was only found in two adult females and in none of the males, with a prevalence of 0.2% of the adult population. Subclinical hypothyroidism was found in 3.8% of the adults. Thus, the overall prevalence of both overt and subclinical hypothyroidism was slightly, but not significantly, lower than that recalculated from the Whickham survey (0.5% and 5.3%, respectively) (1, 2, 3).
Humoral and echographic evidence of diffuse autoimmune thyroiditis was found in 3.5% of the entire population; women over the age of 45 yr were more frequently affected. Most of these subjects were clinically and biochemically euthyroid, and about half of them had an enlarged thyroid gland. To our knowledge, no epidemiological study using thyroid antibody tests combined with ultrasound for the assessment of thyroid autoimmunity has been performed as yet. In agreement with previous studies performed in iodine-deficient areas (29, 30), the detection of serum thyroid antibodies was relatively frequent, especially in goitrous females. Antibody titers were low in most cases and were not associated with thyroid functional alterations or with diffuse autoimmune thyroiditis, as assessed by ultrasound. This finding is in keeping with the concept that the development of goiter due to iodine deficiency may overexpose the immune system to thyroid antigens, leading to humoral and cell-mediated immune reactions (29, 30, 31, 32).
The question of whether iodine intake influences the development of thyroid cancer remains controversial (33). In the present survey only a single case of papillary thyroid carcinoma was found. Although a number of surgical and autopic (34, 35, 36, 37) data on the relationship between iodine intake and thyroid cancer are available, to our knowledge no comparable epidemiological studies have been performed in iodine-deficient areas. The size of the iodine-deficient community examined by us is not sufficient to draw any conclusion. Clearly, more extensive studies are required to address this problem.
In conclusion, the present survey performed in virtually the entire population of a village with mild to moderate iodine deficiency shows a cross-sectional picture of the spectrum of thyroid disorders occurring in iodine deficiency and provides relevant information on the natural history of iodine-deficient goiter. In the present survey of an iodine-deficient community, a progressive increase with age in goiter prevalence, thyroid nodularity, and functional autonomy was observed. Hyperthyroidism was twice as high as that reported in iodine-sufficient areas, mainly due to an increased frequency of toxic nodular goiter. Although low titer serum thyroid antibodies were relatively frequent, the prevalence of both overt and subclinical autoimmune hypothyroidism was not different from that observed in iodine-sufficient areas.
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Acknowledgments |
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Footnotes |
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Received February 4, 1998.
Revised September 30, 1998.
Accepted November 12, 1998.
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