Thyroid Dysfunction in Isolated Adrenocorticotropic Hormone (ACTH) Deficiency: Case Report and Literature Review
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1 Endocrine Journal 1993, 40 (4), NOTE Thyroid Dysfunction in Isolated Adrenocorticotropic Hormone (ACTH) Deficiency: Case Report and Literature Review TAKEHIKO MURAKAMI, SEIKI WADA, YASUYUKI KATAYAMA, Yoxo NEMOTO, NoBUo KUGAI, AND NAOKAZU NAGATA The Third Department o f Internal Medicine, National Defense Medical College, Saitama 359, Japan Abstract. A case of isolated ACTH deficiency accompanying transient primary hypothyroidism was reported along with a review of literature on isolated ACTH deficiency in Japan with special reference to its association with thyroid function. Our case, a 56-year-old woman, developed somnolence and hypoglycemia due to isolated ACTH deficiency. She also had the features of hypothyroidism, namely mounding phenomenon, muscle rigidity, increased plasma myogenic enzymes and cold intolerance. Both free T3 and free T4 were decreased, and basal as well as TRH-stimulated TSH levels were abnormally high. Plasma thyroglobulin was increased and no anti-thyroid antibodies were detected. All thyroid related physical and biochemical abnormalities disappeared after hydrocortisone replacement. A review of the literature on 103 cases disclosed that more than half the cases with isolated ACTH deficiency had a high plasma level of TSH, basal and/or TRH-induced, while the antithyroid antibodies were reported to be positive in only 13 cases. In more than 70% of such cases, the abnormality in the pituitary-thyroid axis was transient and was reversed by glucocorticoid replacement. Our case and cases in the literature indicate that the interference of thyroid hormone synthesis and/or secretion by glucocorticoid deficiency per se is the major cause of thyroid dysfunction rather than associated autoimmune thyroid disease. Key words: Isolated ACTH deficiency, Primary hypothyroidism, Pituitary-thyroid axis. (Endocrine Journal 40: , 1993) SINCE Steinberg et al. first reported isolated ACTH deficiency in 1954 [1], more than 200 cases have been reported in Japan, and many cases are known to accompany thyroid hormone abnormalities [2]. A considerable number of patients with isolated ACTH deficiency have been proven to possess circulating autoantibodies to pituitary cells [2, 3], and the disease is presumed to be induced, at least partly, by an autoimmune mechanism as Received: January 29, 1993 Accepted: May 21, 1993 Correspondence to: Dr. Seiki WADA, The Third Department of Internal Medicine, National Defense Medical College, 3-2 Namiki, Tokorozawa, Saitama 359, Japan proposed previously by Richtsmeier et al. [4]. Although thyroid dysfunction encountered frequently in this disorder has been generally believed to be caused by associated autoimmune abnormalities [5, 6], Topliss [7] and Mashito [8] disclosed that cortisol deficiency itself could affect the pituitary-thyroid axis. In this report, we show a case of isolated ACTH deficiency accompanied by thyroid hormone abnormality, and review the literature on isolated ACTH deficiency in Japan. It was intended to make clear whether or not the autoimmune mechanism was the dominant mechanism causing thyroid dysfunction in this disorder.
2 474 MURAKAMI et al. Case Report A 56-year-old woman was first admitted to our hospital because of loss of consciousness and muscle rigidity. Before admission, she had complained of general fatigue and poor appetite, and had lost 14 kg in weight over the preceding 5 months. Examination on admission showed emaciation with a body weight of 40 kg and a height of 156 cm. She was somnolent and disoriented. Body temperature was 38.2 C, pulse was 60/min, and blood pressure was 128/76 mmhg. No hyperpigmentation was observed on the skin or mucosa. The breasts were atrophic, the pubic hair was scanty, and no axillary hair was visible. The thyroid gland was normal in size and consistency. She had muscle rigidity, and mounding phenomenon was observed on bilateral forearms, but there was neither pitting nor non-pitting pretibial edema. Nuchal stiffness and Kernig's sign were unclear. Blood chemistry revealed hypoglycemia (blood glucose 29 mg/dl), slightly increased musclederived enzymes [creatine kinase 224 U/L (normal 0-160), aldolase 3.4 U/L (normal )], but serum electrolytes were within the normal range. Hematological test showed a slight increase in the number of white blood cells (8900/µl) with 8% of eosinophels. The erythrocyte sedimentation rate was 88 mm/1 h and C-reactive protein was 6.3 mg/dl. The spinal fluid was normal. Basal endocrinological data are shown in Table 1 and the results of various dynamic tests are shown in Figs. 1 and 2. Autoantibodies to the pituitary cell, measured according to the method of Sugiura et al. [3], were positive for both AtT-20 and GH3 cells. Anti-microsomal (microsome hemoagglutinin), anti-thyroglobulin (thyroglobulin hemoagglutinin), and TSH receptor antibodies were all negative. Sagittal section on magnetic resonance imaging (MRI) of the head revealed empty sella. Among pituitary hormones only ACTH was found to be deficient, and a diagnosis of isolated ACTH deficiency was made. The clinical symptoms gradually improved after the provision of supportive care including antibiotics, and improved markedly after hydrocortisone replacement (15 mg/day) was started. Without giving thyroid hormone, abnormalities of muscle supposedly related to hypothyroidism improved along with the normalization of biochemical parameters of thyroid function as shown in Fig. 3. Literature survey We reviewed, with special attention to the associated thyroid dysfunction, the reports on isolated ACTH deficiency in Japan. We were able to evaluate 103 cases with sufficient hormonal data. The age of the patients ranged from 14 to 80 years old with an average of 51.3 years, and the male/female ratio was 1/3. Among these cases, 54 Table 1. Endocrinological findings
3 ACTH DEFICIENCY AND THYROID 475 Fig. 1. Anterior pituitary and adrenal function tests before hydrocortisone replacement (A): rapid ACTH test (Cosyntropin, 250 µg iv), (B): TRH stimulation test (Protirelin, 500 µg iv), (C): LH-RH stimulation test (Gonadorelin, 100 µg iv), and (D): Arginine stimulation test (L-arginine, 0.5 g/kg iv). Fig. 2. CRH stimulation test. (A) A single dose of 100 mg of ovine CRH iv was administered. (0): ACTH; ( ): cortisol. (B) After the iv administration of 100 mg of ovine CRH once daily for 3 consecutive days, CRH stimulation test was repeated. (0): ACTH; ( ): cortisol. cases were detailed on thyroid antibodies, and 13 cases were documented as positive. We classified the cases into three major groups according to the state of the pituitary-thyroid axis, as shown in Table 2. The axis appeared normal in 39.8% of cases (41 cases) (Group A). Increased basal TSH or increased TSH response to TRH was observed in 45.6% of cases (47 cases) (Group B). In this group, about one half (22 cases) had normal thyroid hormone values, and in most of the cases glucocorticoid replacement normalized TSH responsiveness to TRH. Such normalization of TSH dynamics by glucocorticoid replacement was observed in 5 of 8 antithyroid antibody-positive cases, 4 of 5 cases without any apparent thyroid abnormality, and 4 of 5 cases with decreased free T4. No change or a further increase in the TRH-stimulated TSH level was found after replacement in two cases, respectively. The improvement ratio appeared not to correlate with the presence or absence of thyroid-related autoantibodies. In the other 15 cases (Group C), 3 cases were accompanied by hyperthyroidism (Graves'
4 476 MURAKAMI et al. Fig. 3. Changes in pituitary-thyroid axis during time in hospital. Table 2. Classification by data of cases from literature survey disease). Discussion Several interactions between glucocorticoid and pituitary-thyroid axis have been reported [9-12], and it is suggested that the physiological concentration of glucocorticoid has a suppressive effect on TSH secretion. Glucocorticoid deficiency may therefore be one of the causes of the increase in basal TSH in isolated ACTH deficiency. The case presented here was diagnosed as one of isolated ACTH deficiency, according to the typical endocrinological findings and positive tests for the autoantibodies to pituitary cells as well as the demonstration of empty sella. We presumed that empty sella would be related to the destruction of pituitary cells by an autoimmune mechanism as proposed by Richtmeier et al. [4]. Initial physical and biochemical abnormalities, i.e., intolerance to cold, mounding phenomenon, and an
5 ACTH DEFICIENCY AND THYROID 477 increase in muscle-derived enzymes may indicate co-existing hypothyroidism. The hypothyroidism did not seem to be associated with autoimmune thyroid disease since the tests for autoantibodies to the thyroid were all negative. Although increased TSH and decreased free T3 and free T4 were consistent with the diagnosis of primary hypothyroidism, the normal level of reverse T3 in the face of decreased thyroid hormones would indicate a co-existing euthyroid sick state. From our literature survey, cases with increased basal TSH or TSH hyperresponsive to TRH comprised about one-half of the cases of isolated ACTH deficiency (Table 2), and increased TSH levels were observed even in cases with normal thyroid hormone. In this review of 103 cases, only 13 cases (12.6%) were documented to be positive in antithyroid antibodies. Autoimmune thyroiditis is fairly common in Japanese women, and about 10-20% of the female population and about 5% of the male are positive for the anti-microsomal and/or anti-thyroglobulin antibody [13]. It is therefore unlikely that the prevalence of autoimmune thyroid disease among patients with isolated ACTH deficiency is significantly higher than that in the general Japanese population, although one investigator has reported about a 20-30% frequency of positive autoantibody to thyroid [2]. Among the cases in Group B for which a detailed follow-up study of pituitary-thyroid function was available (18 cases), 72% of the patients showed that increased TSH and hyperresponsiveness to TRH could be improved after glucocorticoid replacement. These transient abnormalities in glucocorticoid deficient patients have been noted previously [14-17], and Topliss recommended that thyroid status should be reassessed after replacement [7]. In our case, high levels of thyroglobulin on admission decreased along with serum TSH after hydrocortisone replacement, and free T3 and free T4 increased inversely (Fig. 3). These sequential changes might indicate that the thyroid had been stimulated by TSH but could not respond normally with thyroid hormone synthesis and secretion while the glucocorticoid deficiency was severe. The decrease in TSH and increases in free T3 and free T4 after hospitalization were observed prior to the replacement. This may be due to the relative amelioration of glucocorticoid deficiency by relieving acute stress mainly caused by infection, as observed previously by Dexter [18]. Although pharmacological doses of glucocorticoids have been reported to depress serum T3 in man [17, 19] and to inhibit iodide uptake into FRTL-5 rat thyroid cells [9], this case as well as cases in the literature may indicate that a physiological dose of glucocorticoid is needed for the synthesis or secretion of thyroid hormone under stimulation by TSH. Furthermore, none of the patients with a normal pituitary-thyroid axis was reported as possessing antithyroid antibodies, whereas cases with pituitary-thyroid abnormality had a high incidence of these antibodies (Table 2). This may indicate that glucocorticoid affects thyroid hormone synthesis and/or secretion more easily in patients with intrinsic thyroid disease Steinberg A, Sheehter FR, Segal HI (1954) True pituitary Addison's disease--a pituitary unitropic deficiency. J Clin Endocrinol Metab 14: Hashimoto K, Nishioka T, Iyota K, Nakayama T, Itoh H, Takeda K, Takamatsu K, Numata Y, Ogasa T (1992) Hyperresponsiveness of TSH and References prolactin and impaired responsiveness of GH in Japanese patients with isolated ACTH deficiency. Folia Endocrinol Japon 68: (In Japanese). Sugiura M, Hashimoto A, Shizawa M, Tsukada M, Saito T, Hayami H, Maruyama S, Ishido T (1987) Detection of antibodies to anterior pituitary cell surface membrane with insulin dependent diabetes mellitus and adrenocorticotropic hormone de ficiency. Diabetes Res 4: Richtsmeier AJ, Henry RA, Bloodworth JMB, Ehrlich EN (1980) Lymphoid hypophysitis with selective adrenocorticotropic hormone deficiency. Arch Intern Med 140: Kamijo K, Kato T, Saito A, Kawasaki K, Suzuki M, Yachi A (1982) A case with isolated ACTH deficiency accompanying chronic thyroiditis. Endocrinol Japon 29(2): Kojima I, Nejima I, Ogata E (1982) Isolated adrenocorticotropin deficiency associated with polyglandular failure. J Clin Endocrinol Metab 54: Topliss DJ, White EL, Stockigt JR (1980) Significance of thyrotropin excess in untreated primary
6 478 MURAKAMI et al adrenal insufficiency. J Clin Endocrinol Metab 50: Mashito T, Takada I, Kenbo T, Tokuhiro H, Watanabe A (1981) Anterior pituitary function before and after treatment in four patients with isolated ACTH deficiency. Nihonnaikagakkaizasshi (J Jpn Soc Intern Med) 70: (In Japanese). Saji M, Kohn LD (1990) Effect of hydrocortisone on the ability of thyrotropin to increase deoxyribonucleic acid synthesis and iodide uptake in FRTL-5 rat thyroid cells: Opposite regulation of adenosine 3', 5'-monophosphate signal action. Endocrinology 127: Re RN, Kourides IA, Ridgway EC, Weintraub BD, Maloof F (1976) The effect of glucocorticoid administration on human pituitary secretion of thyrotropin and prolactin. J Clin Endocrinol Metab 43: Otsuki M, Sakoda M, Baba S (1973) Influence of glucocorticoids on TRF-induced TSH response in man. J Clin Endocrinol Metab 36: Nicoloff JT, Fisher DA, Appleman MD Jr (1970) The role of glucocorticoid in the regulation of thyroid function in man. J Clin Invest 49: Amino N (1990) The cause and the pathogenesis of Hashimoto's thyroiditis. Nihonnaikagakkaizasshi (J Jpn Soc Intern Med) 79: (In Japanese). 14. Gharib H, Hodgson SF, Gastineau CF, Scholz DA, Smith LA (1972) Reversible hypothyroidism in Addison's disease. Lancet 2: Candrina R, Giustina G (1987) Addison's disease and corticosteroid-reversible hypothyroidism. J Endocrinol Invest 10 : Proto G, Bertolissi F (1988) Reversible hypothyroidism in idiopathic adrenal insufficiency and in isolated ACTH deficiency. J Endocrinol Invest 11: Duick DS, Warren DW, Nicoloff JT, Otis CL, Croxson MS (1974) Effect of single dose dexamethasone on the concentration of serum triiodothyronine in man. J Clin Endocrinol Metab 39: Dexter RN (1990) Hypopituitarism. In: Becker KL (ed) Principles and Practice of Endocrinology and Metabolism. J. B. Lippincott Company, Philadelphia pp Degroot LJ, Hoye K (1976) Dexamethasone suppression of serum T3 and T4. J Clin Endocrinol Metab 42:
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