A Case of Hypo-Responsiveness to Thyroid Hormone
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1 Clin Pediatr Endocrinol 1996; 5(1): Copyright 1996 by The Japanese Society for Pediatric Endocrinology A Case of Hypo-Responsiveness to Thyroid Hormone Yumi Kitazawa, Tetsuo Mori, Yukio Sekiguchi, Shigeyuki Matsuzawa, Atsushi Baba, Kazuhiko Washizawa, Yasunobu Wakabayashi, Atsushi Komiyama, Akihiro Sakurai and.. Kiyoshi Hashizume Department of Pediatrics, Nagano Red Cross Hospital, (YK, YS, SM, AB, KW YW), Shinshu University School of Medicine, (TM, AK), Department of Geriatrics, Endocrinology and Metabolism, Shinshu University School of Medicine, (AS, KH), Nagano, Japan Abstract A 16-month-old male patient with severe growth and mental retardation is reported. Although his thyroid function tests showed high circulating levels of free 3,5,3'-triiodothyronine (T3), free thyroxin (T4) and thyrotropin (TSH), he had no clinical manifestations suggesting hyperthyroidism. Physical responses to exogenous T3 were normal. T4 supplement (7-10ƒÊg/kg/day) dramatically improved his growth and mental development, suggesting that his clinical symptoms were due to a relative shortage of thyroid hormone. Direct sequencing confirmed that he carried a normal thyroid hormone receptor ƒà (TRƒÀ) gene. The mechanism causing hypo-responsiveness to thyroid hormone in this patient is unclear. Key Words: hypothyroidism, growth retardation, resistance to thyroid hormone Introduction Thyroid hormones exert important effects on the control of metabolic rate and oxygen consumption. Decreased thyroid hormone production results in decreased protein synthesis and decreased cell metabolism, with various effects on intermediary metabolism (1). During early postnatal life, infants with thyroid hormone deficiency gradually develop the clinical manifestations of congenital cretinism such as thermogenic and metabolic dysfunction, and growth failure. Prolonged hypothyroidism delays neuronal maturation and results in irreversible mental retardation (2). Newborn screening for congenital hypothyroidism is now routine in many countries including Japan, and has been highly successful in identifying infants with elevated levels of thyrotropin (TSH)(3). For these infants with high TSH, replacement therapy with thyroxine (T4) should be started after confirmation of low levels of thyroid hormones. We recently encountered a 16-month-old Received: May 22, 1995 Accepted: October 25, 1995 Correspondence: Dr. Akihiro Sakurai. Department of Geriatrics, Endocrinology and Metabolism, Shinshu University School of Medicine, Asahi, Matsumoto-shi, Nagano 390 Japan boy with clinical manifestations of hypothyroidism such as growth and mental retardation, inactivity, and hypotonia. Although he was negative in neonatal screening, his TSH level was significantly high, implying that his clinical 17
2 Vo1.5INo.1 Kitazawa et al. manifestations might be due to primary hypothyroidism. However, his thyroid hormone levels were not decreased, but were rather higher than the normal range. His clinical symptoms were ameliorated by the administration of T4. Discordance between TSH and thyroid hormone levels (inappropriate secretion of TSH: SITSH) is observed in several uncommon pathological conditions, but none of these applied to him. Case Report The patient, a 16-month-old boy (birth date, January 27, 1993), was referred to our hospital because of severe growth and mental retardation. He was born to non-consanguinous parents at 36 weeks gestation (2,650 g, 50 cm). The pregnancy, birth and neonatal period were uncomplicated. On admission, his height was 63 cm (-5.4 standard deviation (SD)), and weight was 6.5 kg (-3.5 SD). His developmental age was compatible with 4 months. He could not sit up, roll over, crawl or speak a word. Bone age estimated by the Greulich and Pyle method was 2 months. Chromosomal analysis showed a normal karyotype of 46, XY. Thyroid function test revealed elevated levels of thyroid hormones and TSH (Table 1), but he had no clinical signs of hyperthyroidism such as tachycardia, hyperhydrosis or diarrhea. Goiter was not detected and 24 h radioiodide uptake was 15.6 %. Scintigraphic imaging showed a normotopic thyroid gland. His mother and maternal grandmother had a history of goiter during pregnancy, but thyroid function tests of his family were unremarkable. Antibodies against 3,5,3'-triiodothyronine (T3) and T4 were negative, and MRI did not show any abnormal findings in the pituitary. High levels of the unbound form of thyroid hormone ruled out any abnormality of thyroid hormone transport. Not only did he lack the clinical manifestations of hyperthyroidism, but he rather showed signs of hypothyroidism, such as growth and mental retardation and hypotonia. The possibility of resistance to thy- Table 2 Results of T3 a ' 'stration test Table 1 Thyroid function tests of family members a Values are for adult subjects. In prepubertal children, normal values for total T3 and total T4 are higher than in adults, largely owing to higher TBG concentration (4, 5). T3 administration test was performed following the protocol of the University of Chicago (6). Dose of T3 was reduced to 25 % of that for adults. It was given as a split dose every 12 hours (8 AM and 8 PM) for three days. Twelve hours after the final administration, blood was drawn for the measurement of thyroid hormone and TSH, and 125, tg of TRH was injected intravenously. TSH was measured every 30 min after injection to 2 hours. Peak value of TSH after TRH injection is shown in the table (TSH-peak). 18
3 June 1996 Hypo-Responsiveness to Thyroid Hormone roid hormone (RTH) was therefore considered, and a T3 administration test was performed (6). Results are summarized in Table 2. After administration of incremental doses of T3, his circulating serum free T3 accordingly rose up to more than 400 % of the upper limit of normal. Metabolic parameters of peripheral thyroid hormone action such as total cholesterol and creatine kinase responded normally to exogenous thyroid hormone. The pulse rate showed only minimal increment, which is not uncommon in normal subjects (6). T4 administration (10 µg/kg/day) was initiated in June, 1994, and an immediate and dramatic improvement was seen in his development and growth. In July, 1994, only one month after the initiation of T4 supplement, he could stand with aid, and his developmental age advanced to 9-10 months. In September, 1994, the results of his thyroid function test were as follows: TSH 0.18 mu/l, total T ng/ml, free T3 5.6 pg/ml, total T418.7,ug/dL, free T ng/dl (normal range of each assay is shown in Table 1). hormones are mostly found in patients with autoimmune thyroid disease, especially those with a high titer of antithyroglobulin antibody (14). In our patient, the presence of anti-thyroid hormone antibodies was ruled out. Although unknown substances other than autoantibody could also interfere with the measurement of thyroid hormone, this possibility is unlikely in our case, since measured free T4 declined proportionally levels of free T3 and to dilution of serum (data not shown). A defect of type I 5'- deiodinase could theoretically cause high serum T4 in eu- or hypo-thyroid subjects. However, there have been no case reports of such defects. R"sler et al. (8) reported patients with putative type II 5'-deiodinase deficiency, whose hyperthy- Table 3 Causes of inappropriate secretion of TSH (SITSH) Discussion A high serum level of total T4 with high or normal TSH in eu- (hypo-) thyroid subjects can be observed in various pathological conditions, as shown in Table 3. Among these disorders, abnormalities in serum T4 transport (thyroxinebinding globulin (TBG) excess, abnormal thyroxine-binding prealbumin, and familial dysalbuminemic hyperthyroxinemia) can be distinguished from the others by measuring free T4 and total T3, which usually give normal values, or directly measuring serum TBG concentration (10). Antibodies against thyroid a Not genetically confirmed. b Only a theoretical consideration. Some patients show clinical features of hyperthyroidism. 19
4 Vol.5/No.1 Kitazawa et al. roidism with a high level of TSH was normalized by T3 but not by T4. In our case, total and free T3 were elevated as well as T4, suggesting normal deiodination. RTH is a syndrome characterized by impaired clinical and biochemical manifestations of thyroid hormone action relative to the circulating hormone levels (6). Recent advances in molecular biology have disclosed that this syndrome is the consequence of a genetic defect in thyroid hormone /3 receptor (TRJ3). In all but one family so far studied, RTH is inherited in an autosomal dominant trait, due to "dominant negative" inhibition by mutant TRJ3 of the function of wild-type TR (15). All reported mutations identified in RTH subjects cluster between exon 7 and exon 10 of the TR/3 gene (6,16). The T3 administration test is a useful procedure for the diagnosis of RTH. Administration of incremental doses of T3 to normal subjects produces significant changes in various parameters which represent peripheral thyroid hormone action. These parameters include total cholesterol, creatine kinase, sex hormone binding globulin and TSH. In subjects with RTH, the changes of these parameters are reduced. We performed the T3 administration test according to the protocol used at the University of Chicago (6). Our patient responded normally to exogenous T3. We also examined the TRJ3 gene of this patient by direct sequencing, using an automated deoxyribonucleic acid (DNA) sequencer. We analyzed exons 4 through 10 of the TRJ3 gene, but no mutations were found in exons or exon-intron boundaries examined (data not shown). The reason for hypo-responsiveness to thyroid hormone in our patient is unclear at this moment. It is also puzzling that he responded normally to exogenous thyroid hormone. The bioactivity of his endogenous thyroid hormone should be examined. It is also unclear whether there may be a relation between his abnormal thyroid function and the histories given by his mother and maternal grandmother of goiters during pregnancy. Careful family study is necessary to elucidate these questions. Finally, concerning supplement therapy to this patient, it is crucial to monitor his growth and development and minimize the dose of T4, since overtreatment with thyroid hormone will facilitate bone maturation and cause premature closure of the epiphyses, which could result in short stature. References 1. Utiger RD, Hypothyroidism. In: DeGroot LJ, editor. Endocrinology Philadelphia: WB Saunders 1994: Fisher DA, The thyroid. In: Brook C, editor. Clinical paediatric endocrinology. Oxford: Blackwell Scientific Publications 1989: Fisher DA, Dussault JH, Foley TP, Klein All, LaFranchi S, Larsen PR, et al, Screening for congenital hypothyroidism: Results of screening one million North American infants. J Pediatr 1979; 94: Fisher DA, Polk DH, Thyroid disease in the fetus, neonate, and child. In: DeGroot LJ, editor. Endocrinology Philadelphia: WB Saunders 1994: Stubbe P, Gatz J, Heidemann P, Muhlen A, Hesch R. Thyroxine-binding globulin, triiodothyronine, thyroxin and thyrotropin in newborn infants and children. Horm Metab Res 1978;10: Refetoff S, Weiss RE, Usala SJ. The syn- 20
5 June 1996 Hypo-Responsiveness to Thyroid Hormone dromes of resistance Endocr Rev 1993;14: to thyroid hormone. 7, Gesundheit T, Petrick PA, Nissim M, Dahlberg PA, Doppman JL, Emerson CH, et al. Thyrotropin-secreting pituitary adenomas: Clinical and biochemical heterogeneity. Case report and follow-up of nine patients. Ann Intern Med 1989;111: Rosier A, Litvin Y, Hage C, Gross J, Cerasi E. Familial hyperthyroidism due to inappropriate thyrotropin secretion successfully treated with triiodothyronine. J Clin Endocrinol Metab 1982; 54: Wartofsky L, Burman KD. Alterations in thyroid function in patients with systemic illness: the "euthyroid sick syndrome." Endocr Rev 1982; 3: Refetoff S. Inherited thyroxine-binding globulin abnormalities in man. Endocr Rev 1989;10: Ruiz M, Rajatanavin R, Young RA, Taylor C, Brown R, Braverman LE et al. Familial dysalbuminemic hyperthyroxinemia: a syndrome that can be confused with thyrotoxicosis. N Engl J Med 1982; 306: Moses C, Lawlor J, Haddow J, Jackson IMD. Familial euthyroid hyperthyroxinemia resulting from increased thyroxine binding to thyroxine-binding prealbumin. N Engl J Med 1982; 306: Sakata S, Nakamura S, Miura K. Autoantibodies against thyroid hormones or iodothyronine. Implications in diagnosis, thyroid function, treatment and pathogenesis. Ann Intern Med 1985;14: Staeheli V, Vallotton MB, Burger A. Detection of human anti-thyroxine antibodies in different thyroid conditions. J Clin Endocrinol Metab 1975; 41: Sakurai A, Miyamoto T, Refetoff S, DeGroot LJ. Dominant negative transcriptional regulation by a mutant thyroid hormone receptor-Ĉin a family with generalized resistance to thyroid hormone. Mol Endocrinol 1990; 4: Refetoff S, weiss RE, Usala SJ, Hayashi Y, The syndromes of resistance to thyroid hormone: Update In: Negro-Vilar A, editor. Endocrine reviews monographs, 3: Clinical and molecular aspects of diseases of the thyroid, Bethesda: Endocr Soc,1994:
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