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The Journal of Clinical Endocrinology & Metabolism Vol. 86, No. 2 750-754
Copyright © 2001 by The Endocrine Society

Original Studies

Sex-Dependent Variations and Timing of Thyroid Growth during Puberty1

Yvan Fleury, Guy Van Melle, Virgile Woringer, Rolf C. Gaillard and Luc Portmann

Division of Endocrinology, Diabetology and Metabolism, Department of Internal Medicine, Centre Hospitalier Universitaire Vaudois (Y.F., R.C.G., L.P.), Institute for Social and Preventive Medicine, University of Lausanne (G.V.M.), and School Health Service (V.W.), CH-1011 Lausanne, Switzerland

Address correspondence and requests for reprints to: Dr. Luc Portmann, Division of Endocrinology, Diabetology and Metabolism, Department of Internal Medicine, Centre Hospitalier Universitaire Vaudois, BH 10, CH-1011 Lausanne, Switzerland.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Marked changes in thyroid function occur during puberty as an adaptation to body and sexual development. Characteristics of thyroid growth were investigated in 259 healthy adolescents (110 girls and 149 boys), aged 11–17 yr, in an urban area of Switzerland with sufficient iodine supply. The thyroid volume determined by ultrasonography was correlated with chronological age, body weight, body height, cervical circumference, body mass index, and body surface area (BSA). Iodide concentration was measured in urine.

The increase in thyroid volume mainly occurred between 11–15 yr (age at maximum thyroid growth rate, 12.5 yr) and was best correlated with BSA in both genders (girls, r2 = 0.38; boys, r2 = 0.49). The BSA-related thyroid growth was almost constant throughout puberty in boys and similar in girls up to menarche, but 14.5% larger in girls after menarche (P < 0.01). Percentiles of thyroid volume were lower than WHO reference values despite low normal urinary iodide concentration (median, 0.75 µmol/L).

These findings suggest that physiological thyroid growth during puberty is mainly influenced by growth factors involved in somatic development and further modulated by sex steroid secretion profiles. The thyroid growth spurt coinciding with menarche in girls may contribute to a higher incidence of goiter during mid- to late puberty.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
THE ONSET OF puberty occurs with the maturation of the hypothalamo-pituitary-gonadal axis, resulting in the development of secondary sexual characteristics, changes in skeletal size, and body composition. Adaptations of the hypothalamo-pituitary-thyroid gland axis in response to the increased energy expenditure have been suggested. A prepubertal surge of TSH between 9.0 and 9.5 yr, followed by a transient increase in circulating thyroid hormones (T4 and T3), in addition to enhanced peripheral conversion of T4 to T3, may account for this adaptation (1). With ongoing puberty, however, decreasing or constant TSH levels have been reported, as well as a progressive decrease in circulating thyroid hormones (1, 2, 3). The increase in thyroid volume that is concurrent with the onset of puberty could be triggered by the reported transient TSH surge, but additional factors may be involved in thyroid stimulation until adulthood. Sustained thyroid growth has been demonstrated by the positive correlation between thyroid size and various determinants such as chronological age, pubertal stage, body weight, body height, and body surface area (BSA; Refs. 4, 5, 6, 7, 8). Although some authors did not find any difference in thyroid volume between genders (4, 5), a larger thyroid gland in girls has been reported by others (6, 7, 8). Sex-related variations are consistent with the observation that thyroid disorders are more frequent in females than in males and particularly occur during puberty and pregnancy, with changes in levels of sex steroids.

The aim of the present study was to determine the gender-specific characteristics of thyroid growth in healthy adolescents living in an area with sufficient iodine supply (9, 10). The thyroid volume measured by ultrasonography was correlated with chronological age and anthropometric parameters.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Three hundred forty-eight representative adolescents (160 girls and 188 boys), aged 11–17 yr (median, 13.8), were examined in this cross-sectional study performed between April and June 1995 in the urban area of Lausanne, Switzerland. All subjects were attending a public secondary school. The present analysis was restricted to the 279 adolescents (126 girls and 153 boys) having exclusively lived in Switzerland, where the iodine supply has been sufficient since 1980 (9, 10). None of the subjects had any evidence of acute or chronic disease, and no previous thyroid disorder was reported. Five girls taking oral contraceptives were excluded. None of the subjects took other medications affecting thyroid function. Twenty adolescents (9 girls and 11 boys) were light cigarette smokers. Thyroid abnormalities were identified by ultrasonography in 15 subjects (11 girls and 4 boys) who were excluded: goiter (n = 4), nodule (n = 8), and diffuse echostructure abnormality (n = 3). Epidemiological results have been detailed elsewhere (11). The clinical characteristics of the 259 adolescents (110 girls and 149 boys) finally included are shown in Table 1Go. Menarche had occurred in 60 girls, of whom 54 had regular menstrual cycles.


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  		Table 1. Clinical characteristics of adolescents

 
Study protocol

Anthropometric measurements and ultrasonography of the thyroid gland were performed in the morning between 0830 and 1200 h. Urine samples were collected at the same time. All subjects had their regular diet and physical activity before examination. The protocol was approved by the ethics committee of the Department of Medicine. All adolescents, as well as their parents, had given written informed consent.

Anthropometric measurements

Adolescents were examined in light clothing without shoes by the same investigator. Body weight (wt), body height (ht), and cervical circumference at the level of the crico-thyroid ligament were measured. Body mass index (BMI) was defined as the weight (in kilograms) divided by the height (in meters) squared. BSA was estimated from the height (in centimeters) and the weight (in kilograms): BSA = 0.007184 x ht0.725 x wt0.425 (12).

Ultrasonography

The thyroid volume was determined by real-time ultrasonography in each adolescent lying supine with the neck hyperextended. Measurements were performed by the same experienced investigator (L.P.) using a Hitachi EUB-405 scanner with a 7.5-MHz, 6.25-cm linear transducer (Hitachi Medical Co., Tokyo, Japan). The length (l), width (w), and depth (d) of each thyroid lobe (in centimeters) were measured on transverse and longitudinal scans. The volume (vol) of each lobe (in milliliters) was estimated by the modified formula of the rotation ellipsoid (vol = l x w x d x 0.479), as described by Brunn et al. (13). The thyroid volume was defined as the sum of the volumes of both lobes. The within-day mean coefficient of variation was 5.8%, and the between-day mean coefficient of variation was 5.9% for determinations performed in five male volunteers. Results were compared with the reference values recommended by the WHO and the International Council for Control of Iodine Deficiency Disorders (ICCIDD) (8).

Urinary iodine

First-morning urine samples were stored at -20 C until assayed. The iodine concentration in urine was measured in duplicate by the same person (Y.F.) using a manual spectrophotometric method based on the Sandell-Kolthoff reaction, as described by Dunn et al. (14). Slight modifications of analytical parameters (200-µL urine samples, constant temperature of 24 C during catalysis) were made to improve the performance in the concentration range of 0.12–2.37 µmol/L (conversion in conventional units: 1 µmol/L = 12.66 µg/dL). At mean iodine concentrations of 0.31, 0.64, and 1.02 µmol/L, the intra-assay coefficients of variation were 4.8%, 2.3%, and 1.9%, respectively, and the interassay coefficients of variation were 5.2%, 4.0%, 2.7%, respectively. Results were assessed according to WHO criteria (15).

Statistical analysis

Data are presented as the mean ± SE, unless otherwise noted. Thyroid volume values were logarithmically transformed. The Kolmogorov-Smirnov test was used to ensure that variables did not significantly differ from a normal distribution. Correlation between thyroid volume and independent variables was assessed in simple and multiple linear regression analysis. Coefficients of determination (r2) were adjusted for each group size. Percentiles of thyroid volume were determined in nonlinear regression analysis using a logistic model:

where y is the logarithm of thyroid volume, x is the independent variable, y0 represents the thyroid volume at the onset of puberty, and x0 corresponds to the x value at which 50% of the pubertal thyroid growth was completed. The slope of the function is an estimate of the thyroid growth rate. The regression represents a symmetric distribution with the mean corresponding to the 50th percentile (P50). The prediction interval between the 5th and 95th percentiles (P5–P95) is the mean ± 1.645 SE. Regression analyses were performed with the SigmaPlot 5.0 program (SPSS, Inc., Chicago, IL). Differences between regression lines or curves were tested by ANOVA. Comparisons between groups were performed by the Mann-Whitney U test. The level of significance was set at 0.05.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
A significant difference in clinical characteristics between genders was found for body height, BMI, and cervical circumference, whereas chronological age, body weight, and BSA were similar (Table 1Go). Morphological disparities mainly occurred during late puberty. The volume of the thyroid gland significantly increased with chronological age and with each anthropometric parameter in simple linear regression analysis (P < 0.0001). Coefficients of determination were higher in boys than in girls, but a significant sex difference was only found in the correlation with body height, cervical circumference, and BSA (Table 2Go). In both genders, the thyroid volume was best related to BSA. The prediction of thyroid volume was slightly improved (P < 0.05) by additional consideration of chronological age in girls (r2 = 0.40) and cervical circumference in boys (r2 = 0.51). The analyses of thyroid growth data were focused on the relation to chronological age and BSA.


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  		Table 2. Determinants of thyroid volume during puberty

 
Thyroid growth and chronological age

The correlation between thyroid volume and chronological age was better in nonlinear (see Subjects and Methods) than in simple linear regression analysis (girls, P < 0.05; boys, P < 0.001). Percentiles derived from the nonlinear regression model were not significantly different between genders (Fig. 1Go). The estimated thyroid size at the onset of puberty was 3.9 mL in girls and 3.5 mL in boys. Fifty percent of pubertal thyroid growth was completed at an estimated age of 12.6 ± 0.6 yr and 12.5 ± 0.3 yr, respectively, which corresponded to the maximum thyroid growth rate. This time point coincided with the age of menarche in girls (Fig. 1Go). The corresponding thyroid volume was 5.4 mL in girls and 4.9 mL in boys. The increase in thyroid size was nearly completed at 15 yr of age, reaching adult values. Percentiles were lower than WHO-ICCIDD reference values in both genders.



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  		Figure 1. Thyroid volume in relation to chronological age. The 5th, 50th, and 95th percentiles (P5, P50, and P95) of thyroid volume were determined after logarithmic transformation of data in nonlinear regression analysis using a logistic model (girls, r2 = 0.30; boys, r2 = 0.38). •, Girls who had had their menarche. The age of menarche is expressed as the mean ± SD. R50 and R97 labels denote the 50th and 97th percentiles of WHO-ICCIDD reference values, respectively (8 ).

 
Thyroid growth and BSA

The BSA-related increase in thyroid size was similar in boys and in girls up to menarche, but significantly larger in girls after menarche (Table 2Go). In multiple linear regression analysis, a 14.5% (95% confidence interval, 5.5–24.1%) increase in thyroid volume was related to the onset of menstrual cycles, resulting in a thyroid growth spurt in girls. The difference in thyroid size between girls in follicular phase (mean ± SD, 6.9 ± 2.2 mL, n = 28) vs. girls in luteal phase (mean ± SD, 8.1 ± 2.7 mL, n = 26) was above the limit of significance (P = 0.07). Percentiles of thyroid volume determined in nonlinear regression analysis showed that 50% of the thyroid growth spurt in girls was completed at 1.50 ± 0.04 m2, whereas the thyroid growth in boys was almost constant throughout pubertal development (Fig. 2Go). In both genders, percentiles were lower than WHO-ICCIDD reference values.



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  		Figure 2. Thyroid volume in relation to BSA. Percentiles (P5, P50, and P95) derived from logarithmically transformed thyroid volume values were determined in nonlinear regression analysis using a logistic model (girls, r2 = 0.40; boys, r2 = 0.49). •, Girls who had had their menarche. R50 and R97 labels denote the 50th and 97th percentiles of WHO-ICCIDD reference values, respectively (8 ).

 
Urinary iodine excretion

Mean ± SD iodine concentration in urine was 0.79 ± 0.37 µmol/L (median, 0.75) with no sex difference. Our findings were consistent with a low normal iodine intake according to WHO criteria. No correlation was found between thyroid volume and urinary iodine.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The increase in thyroid volume during puberty is a normal adaptation that may coincide with the development of goiter in pathological conditions, particularly in girls (6, 7, 8). In the present cross-sectional study, the physiological characteristics of thyroid growth were assessed in healthy Swiss adolescents aged 11–17 yr. The age distribution was ranging from the onset to the late stages of puberty according to Swiss longitudinal pubertal studies (16, 17). The investigation was designed to determine the gender-specific features likely to have a positive influence on the incidence of goiter during puberty.

In both genders, the thyroid volume was best related to BSA, as reported by other authors (7, 8). The somewhat lower correlation between thyroid volume and chronological age may be ascribed to the individual variations commonly seen in the timing of pubertal development. The influence of somatic growth on thyroid size could be affected by changes in body composition as well. The latter is suggested by the fact that males with greater body weight gain have a larger thyroid gland than females in adulthood (18), with lean body mass as a major determining factor (19).

The relationship between pubertal development and the increase in thyroid volume implies that a number of growth factors may have a positive modulation effect on the hypothalamo-pituitary-thyroid gland axis and, possibly, through TSH-independent pathways on the thyroid gland itself. Although decreasing or constant TSH levels in both genders have been reported by some authors (1, 2), these findings did not exclude changes in pulsatile and circadian TSH secretion (20, 21). In addition, growth factors may induce alterations in TSH receptor sensitivity or in other thyroid endogenous pathways (22). In healthy adolescents, the striking rise in GH and insulin-like growth factor I (IGF-I) may contribute to such a modulation. Previous studies have demonstrated that IGF-I potentiates the mitogenic action of TSH in rat (22) and human thyroid cells in culture (23), but has little effect by itself. In vivo stimulation of thyroid growth by IGF-I is supported by the positive correlation between thyroid volume and plasmatic levels of GH/IGF-I in acromegalic patients (24). Accordingly, the sex-dependent patterns of GH secretion (25) may affect the physiological increase in thyroid size during puberty.

The changes in thyroid volume mainly occurred between 11–15 yr, in agreement with previously published data (6, 7). The estimated maximum thyroid growth rate, however, was reached at a similar chronological age in both genders and was related to the age of menarche in girls. With reference to the pubertal stages reported in the Swiss longitudinal studies, this time point would coincide with early to mid-puberty in boys (16) and mid- to late puberty in girls (17). In addition, a thyroid growth spurt was obvious in girls whereas such an alteration was not observed in boys when the thyroid volume was assessed in relation to BSA. These findings suggest that specific features other than somatic changes may contribute to the modulation of thyroid growth. Some investigators also have found that circulating thyroid hormones have a sex-dependent profile during mid- to late puberty, with free T3 levels decreasing in girls but remaining constant in boys, and decreasing total and free T4 levels in both genders, with a slight delay in boys (2, 3). These variations may lead to a distinct feedback regulation of TSH secretion, with differences in frequency and amplitude of pulses, which, in turn, may affect thyroid function.

On the other hand, the gender-specific thyroid growth patterns found in the present study may be related, to some extent, to the changes in sex steroid secretion profiles as suggested by the thyroid growth spurt coinciding with menarche in girls and by the ability of sex steroids to promote a modulation of the hypothalamo-pituitary-thyroid gland axis in experimental studies. A positive effect of estrogens on the adenohypophysis has been demonstrated in the adult rat, resulting in higher density of pituitary T3 and TRH receptors and increased activity of type II 5'-deiodinase, whereas androgens only had a slight inhibitory effect on the latter (26). In human adults, the enhanced TSH response to TRH after administration of estrogens may reflect similar changes in pituitary parameters, in addition to the rise in T4-binding globulin (27). Furthermore, several authors have identified sex steroid receptors in normal and pathological human thyroid tissues and suggested that estrogens might have a positive influence and androgens a rather restraining influence on the thyroid gland itself (28, 29, 30). Taken together, such observations indicate that sex steroids might have a similar modulation effect during puberty in both genders, with potentially more variations in girls. The thyroid growth spurt observed in girls could not be limited to alterations of thyroid size during the follicular and luteal phases because the difference between these two subgroups was not significant. Evidence of menstrual cycle-related changes in thyroid volume has only been reported in adult women living in an area with mild iodine deficiency (31), but not in women with a sufficient iodine intake (32).

In iodine deficiency, the reduced direct inhibitory effect of iodine may enhance the positive influence of factors involved in the physiological regulation of thyroid growth. Furthermore, the sensitivity to TSH is increased, so that normal TSH levels already have a goitrogenic effect (33). The outcome of such a stimulation may be substantial in girls with mild iodine deficiency, leading to the development of goiter during mid- to late puberty. Despite a low normal urinary iodide concentration, such a stimulation was unlikely in the adolescents selected for the present study, because 1.4% of them only were diagnosed with a goiter and percentiles of thyroid volume were lower than WHO-ICCIDD reference values. In addition, previous studies have demonstrated that iodine supply through iodized salt prophylaxis has been sufficient since 1980 in several regions of Switzerland (9). The low normal iodine intake observed in the present study may be attributed to seasonal variations in milk iodine content, which is 0.27–0.71 µmol/kg lower in the summer than in the winter, as suggested by a median urinary iodide concentration of 1.19 µmol/L found in winter 1997 in the same area (10).

In conclusion, the thyroid growth in adolescents with a normal iodine supply is mainly related to changes in BSA in both genders and may result from interactions between the hypothalamo-pituitary-thyroid gland axis and growth factors. The increase in thyroid volume is similar in boys and girls up to the age of menarche, when girls have a distinct thyroid growth spurt, suggesting that female sex steroids might have an additional positive influence on thyroid function as well. As a result, girls might be more susceptible than boys to variations in thyroid volume during mid- to late puberty. These physiological changes may contribute to a higher incidence of goiter in girls with mild iodine deficiency.


   Acknowledgments
 
We thank Drs. F. Pralong, P. Vollenweider, J. Ruiz, and V. Giusti for helpful comments; as well as Ms. E. Temler and Drs. F. Rey, M. J. Reymond, S. Lauper, and M. Riklin for technical assistance. We are grateful to Mr. A. Bouquet and Mr. B. Verrey for help in the organization of the study.


   Footnotes
 
1 Presented in part at the Annual Meeting of the Swiss Endocrine Society, Berne, Switzerland, November 1996. Back

Received January 8, 2000.

Revised October 6, 2000.

Accepted October 17, 2000.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. Michaud P, Foradori A, Rodriguez-Portales JA, Arteaga E, López JM, Téllez R. 1991 A prepubertal surge of thyrotropin precedes an increase in thyroxine and 3,5,3'-triiodothyronine in normal children. J Clin Endocrinol Metab. 72:976–981.[Abstract/Free Full Text]
  2. Parra A, Villalpando S, Junco E, Urquieta B, Alatorre S, Garcia-Bulnes G. 1980 Thyroid gland function during childhood and adolescence. Changes in serum TSH, T4, T3, thyroxin-binding globulin, reverse T3 and free T4 and T3, concentrations. Acta Endocrinol (Copenh). 93:306–314.[Abstract/Free Full Text]
  3. Dunger DB, Perkins JA, Jowett TP, et al. 1990 A longitudinal study of total and free thyroid hormones and thyroxine-binding globulin during normal puberty. Acta Endocrinol. (Copenh). 123:305–310.
  4. Chanoine JP, Toppet V, Lagasse R, Spehl M, Delange F. 1991 Determination of thyroid volume by ultrasound from the neonatal period to late adolescence. Eur J Pediatr. 150:395–399.[CrossRef][Medline]
  5. Ivarsson SA, Persson PH, Ericsson UB. 1989 Thyroid gland volume as measured by ultrasonography in healthy children and adolescents in a non-iodine deficient area. Acta Paediatr Scand. 78:653–654.[Medline]
  6. Gutekunst R, Smolarek H, Hasenpusch U, et al. 1986 Goitre epidemiology: thyroid volume, iodine excretion, thyroglobulin and thyrotropin in Germany and Sweden. Acta Endocrinol (Copenh). 112:494–501.[Abstract/Free Full Text]
  7. Müller-Leisse C, Tröger J, Khabirpour F, Pöckler C. 1988 Schilddrüsenvolumen-Normwerte. Sonographische Messungen an 7-bis 20jährigen Schülern. Dtsch Med Wochenschr. 113:1872–1875.[Medline]
  8. World Health Organization, International Council for Control of Iodine Deficiency Disorders. 1997 Recommended normative values for thyroid volume in children aged 6–15 years. Bull World Health Organ. 75:95–97.[Medline]
  9. Bürgi H, Supersaxo Z, Selz B. 1990 Iodine deficiency diseases in Switzerland one hundred years after Theodor Kocher’s survey: a historical review with some new goitre prevalence data. Acta Endocrinol (Copenh). 123:577–590.[Medline]
  10. Bürgi H, Portmann L, Podoba J, Vertongen F, Srbecky M. 1999 Thyroid volumes and urinary iodine in Swiss school children, 17 years after improved prophylaxis of iodine deficiency. Eur J Endocrinol. 140:104–106.[Abstract]
  11. Fleury Y, van Melle G, Woringer V, Temler E, Gaillard RC, Portmann L. 1999 Apport iodé et prévalence du goitre chez les adolescents dans le canton de Vaud. Schweiz Med Wochenschr. 129:1831–1838.[Medline]
  12. Du Bois D, Du Bois EF. 1916 A formula to estimate the approximate surface area if height and weight is known. Arch Intern Med. 17:863.
  13. Brunn J, Block U, Ruf G, Bos I, Kunze WP, Scriba PC. 1981 Volumetrie der Schilddrüsenlappen mittels Real-time-Sonographie. Dtsch Med Wochenschr. 106:1338–1340.[Medline]
  14. Dunn JT, Crutchfield HE, Gutekunst R, Dunn AD. 1993 Two simple methods for measuring iodine in urine. Thyroid. 3:119–123.[Medline]
  15. Bourdoux P. 1993 Biochemical evaluation of iodine status. In: Delange F, Dunn JT, Glinoer D, eds. Iodine deficiency in Europe. A continuing concern. New York: Plenum Press; 119–125.
  16. Largo RH, Prader A. 1983 Pubertal development in Swiss boys. Helv Paediatr Acta. 38:211–228.[Medline]
  17. Largo RH, Prader A. 1983 Pubertal development in Swiss girls. Helv Paediatr Acta. 38:229–243.[Medline]
  18. Hegedüs L, Perrild H, Poulsen LR, et al. 1983 The determination of thyroid volume by ultrasound and its relationship to body weight, age, and sex in normal subjects. J Clin Endocrinol Metab. 56:260–263.[Abstract/Free Full Text]
  19. Wesche MFT, Wiersinga WM, Smits NJ. 1998 Lean body mass as a determinant of thyroid size. Clin Endocrinol. 48:701–706.[CrossRef][Medline]
  20. Greenspan SL, Klibanski A, Schoenfeld D, Ridgway EC. 1986 Pulsatile secretion of thyrotropin in man. J Clin Endocrinol Metab. 63:661–668.[Abstract/Free Full Text]
  21. Rose SR, Nisula BC. 1989 Circadian variation of thyrotropin in childhood. J Clin Endocrinol Metab. 68:1086–1090.[Abstract/Free Full Text]
  22. Dumont JE, Lamy F, Roger P, Maenhaut C. 1992 Physiological and pathological regulation of thyroid cell proliferation and differentiation by thyrotropin and other factors. Physiol Rev. 72:667–697.[Free Full Text]
  23. Ollis CA, Hill DJ, Munro DS. 1989 A role for insulin-like growth factor-I in the regulation of human thyroid cell growth by thyrotrophin. J Endocrinol. 123:495–500.[Abstract/Free Full Text]
  24. Miyakawa M, Saji M, Tsushima T, Wakai K, Shizume K. 1988 Thyroid volume and serum thyroglobulin levels in patients with acromegaly: correlation with plasma insulin-like growth factor I levels. J Clin Endocrinol Metab. 67:973–978.[Abstract/Free Full Text]
  25. Clark PA, Rogol AD. 1996 Growth hormones and sex steroid interactions at puberty. Endocrinol Metab Clin North Am. 25:665–681.[CrossRef][Medline]
  26. Donda A, Reymond F, Rey F, Lemarchand-Béraud T. 1990 Sex steroids modulate the pituitary parameters involved in the regulation of TSH secretion in the rat. Acta Endocrinol (Copenh). 122:577–584.[Abstract/Free Full Text]
  27. Ramey JN, Burrow GN, Polackwich RJ, Donabedian RK. 1975 The effect of oral contraceptive steroids on the response of thyroid-stimulating hormone to thyrotropin-releasing hormone. J Clin Endocrinol Metab. 40:712–714.[Abstract/Free Full Text]
  28. Mizukami Y, Michigishi T, Nonomura A, Hashimoto T, Noguchi M, Matsubara F. 1991 Estrogen and estrogen receptors in thyroid carcinomas. J Surg Oncol. 47:165–169.[Medline]
  29. Dalla Valle L, Ramina A, Vianello S, Fassina A, Belvedere P, Colombo L. 1998 Potential for estrogen synthesis and action in human normal and neoplastic thyroid tissues. J Clin Endocrinol Metab. 83:3702–3709.[Abstract/Free Full Text]
  30. Rossi R, Franceschetti P, Maestri I, et al. 1996 Evidence for androgen receptor gene expression in human thyroid cells and tumours. J Endocrinol. 148:77–85.[Abstract/Free Full Text]
  31. Hegedüs L, Karstrup S, Rasmussen N. 1986 Evidence of cyclic alterations of thyroid size during the menstrual cycle in healthy women. Am J Obstet Gynecol. 155:142–145.[Medline]
  32. Berghout A, Endert E, Ross A, Hogerzeil HV, Smits NJ, Wiersinga WM. 1994 Thyroid function and thyroid size in normal pregnant women living in an iodine replete area. Clin Endocrinol. 41:375–379.[Medline]
  33. Dumont JE, Ermans AM, Maenhaut C, Coppée F, Stanbury JB. 1995 Large goitre as a maladaptation to iodine deficiency. Clin Endocrinol. 43:1–10.[Medline]



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