Adrenal Tuberculosis in Cushing s Disease with Bilateral Macronodular Adrenocortical Hyperplasia
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1 Endocrine Journal 2006, 53 (2), Adrenal Tuberculosis in Cushing s Disease with Bilateral Macronodular Adrenocortical Hyperplasia HYUK-SANG KWON, SANG-IL KIM, SOON-JIB YOO, KUN-HO YOON, KWANG-WOO LEE, MOON-WON KANG, HO-YOUNG SON, SUNG-KOO KANG AND BONG-YUN CHA Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul , Korea Abstract. Cushing s disease is a disorder of hypercortisolism caused by a pituitary micro- or macro-adenoma. Most patients with Cushing s disease have a bilateral adrenal enlargement, which depends on the duration of the disease, as a result of the long standing ACTH stimulation of both adrenal glands. However, in macronodular adrenocortical hyperplasia (MNH) that is caused by Cushing s disease, if the MNH gains autonomy, a bilateral adrenalectomy, as well as the removal of pituitary adenoma, is often essential. We encountered a patient diagnosed with Cushing s disease with bilateral adrenal tuberculosis simulating MNH. She had taken anti-tuberculosis medications one year prior to admission due to spinal tuberculosis. Sellar MRI revealed a pituitary macroadenoma, but adrenal CT showed enlargement in both adrenal glands that appeared to be MNH. A hormonal study and bilateral inferior petrosal sinus sampling revealed Cushing s disease. Therefore, she underwent trans-sphenoidal surgery of the pituitary mass. The pituitary surgery was successful and the serum cortisol returned to normal range. However, the adrenal mass rapidly enlarged after removing the pituitary tumor without showing evidence of a recurrence or adrenal autonomy of hypercortisolism. Accordingly, a laparoscopic left adrenalectomy was performed to examine the nature of the mass. The resected left adrenal gland was pathologically determined to have a lesion of tuberculosis with some part of the intact cortex. So we assumed that the cause of rapid adrenal enlargement might be due to adrenal tuberculosis. In summary, to the best of our knowledge, this is the first case of Cushing s disease coexisting with both adrenal tuberculosis simulating a bilateral MNH. Key words: Cushing s disease, Macronodular adrenocortical hyperplasia (MNH), Adrenal tuberculosis (Endocrine Journal 53: , 2006) CUSHING S disease is caused by the pituitary hypersecretion of ACTH, and accounts for 70 to 80% of Cushing s syndrome cases. Most patients with pituitary dependent Cushing s syndrome (Cushing s disease) have diffuse bilateral hyperplasia or micronodular hyperplasia. However, macroscopic nodules may be found that sometimes mimick ACTH-independent Cushing s syndrome biochemically or radiologically. Defective adrenal suppression, even by high dexamethasone doses, and scintigraphic lateralization of the adrenal gland in the presence of normal or elevated plasma ACTH levels in patients with long-standing Received: June 10, 2004 Accepted: December 19, 2005 Correspondence to: Bong-Yun CHA, M.D., Ph.D., Kangnam St. Mary s Hospital, The Catholic University of Korea, #505 Banpodong, Seocho-gu, Seoul , Korea Cushing s syndrome may be valuable clues indicating macronodular adrenocortical hyperplasia (MNH) [1]. The pathophysiology and principles for treating MNH associated with Cushing s disease are unclear. Some authors believe that MNH have a potential adrenal autonomy that needs to be treated by adrenalectomy, while others advocate trans-sphenoidal surgery for removing a pituitary adenoma [2]. An adrenal insufficiency due to adrenal cortical destruction is the most common endocrine deficiency caused by a M. tuberculosis infection. Radiographic evidence of adrenal calcification is the most helpful positive diagnostic sign of adrenal tuberculosis, but it is present in only 15% of cases [3]. When coexisting with Cushing s syndrome, the typical symptoms related to Cushing s syndrome might be partially masked by the adrenal insufficiency as a result of adrenal tuberculosis [4].
2 220 KWON et al. This paper describes a patient with Cushing s disease, who had bilateral adrenal enlargements mimicking MNH. The diagnosis of adrenal tuberculosis was made after surgery. Case Report A 34 year old woman visited our endocrinology outpatient clinic complaining of weight gain and fatigue. She had been diagnosed with spinal tuberculosis with pulmonary involvement a year before and underwent orthopedic surgery. She had taken anti-tuberculosis medication (isoniazid, rifampin, ethambutol) and underwent a computed tomography (CT) to assess the response to the therapy several weeks ago. Bilateral adrenal enlargements were detected incidentally from computed tomography of the chest and spine. She had hypertension and diabetes mellitus, which was diagnosed one month ago, but took no medication to control the blood pressure and glucose level. Physical examination revealed her height to be 172 cm; weight, 72 kg; blood pressure, 130/90 mmhg; and body temperature 36 C. She had a moon face, diffuse acne on her face, central obesity and supraclavicular fat-pads. Initial laboratory findings showed a white blood cell count of 8000/mm 3 ; hemoglobin, 13.9 g/dl; hematocrit, 39.9%; and platelets, 304,000/mm 3. Serum sodium level was 148 meq/l; potassium, 3.2 meq/l; and chloride, 101 meq/l. Blood urea nitrogen concentration was 13.0 mg/dl; serum creatinine, 0.85 mg/dl. Fasting plasma glucose level was 179 mg/dl; serum cholesterol, 252 mg/dl; and triglyceride, 290 mg/dl. Plasma ACTH levels were pg/ml in the early morning and pg/ml in the evening, and Serum cortisol levels were g/dl in the early morning and g/dl in the evening. Level of urinary free cortisol excretion was 97.4 g/day (normal range; 0 77). Urinary catecholamine levels were normal. Urinary excretions of 17-KS were 5.8 mg/day, and serum dehydroepiandrosterone sulfate level was g/dl. Her serum cortisol failed to fall during a 1-mg overnight dexamethasone suppression test (postdexamethasone serum cortisol concentration, g/ dl). After a 2-day high dose (2 mg every 6 hr for 2 days) dexamethasone suppression test, her serum cortisol (from to g/dl) and 24 hr urinary free cortisol (from to g/day) failed to fall indicating a pituitary macroadenoma or ectopic ACTH syndrome, which is less likely to be adrenal autonomy (Table 1). Adrenal CT revealed bilateral macronodular hyperplasia (right 5 cm, left 5.5 cm) (Fig. 1). Magnetic resonance imaging (MRI) of the pituitary gland showed a pituitary macroadenoma ( cm) (Fig. 2). Accordingly, bilateral inferior petrosal sinus sampling was performed to confirm the ACTH produc- Table 1. Summary of the results of hormonal studies Hormonal profiles Results Serum cortisol concentration 08:00 AM g/dl 11:00 PM g/dl After 1 mg overnight DST g/dl Serum ACTH concentration pg/ml 24-hour urine free cortisol 97.4 g/day Before high-dose DST g/day After high-dose DST g/day Bilateral inferior petrosal sinus sampling ACTH level (pg/ml) (ratio) Before CRH stimulation (IPS/PB) / (4.52) Before CRH stimulation (Rt/Lt) / (3.80) After CRH stimulation (IPS/PB) / (4.25) After CRH stimulation (Rt/Lt) / (4.05) DST; dexamethasone suppression test, IPS; inferior petrosal sinus, PB; peripheral blood, Rt; right petrosal sinus, Lt; left petrosal sinus Fig. 1. Adrenal computed tomography showing bilateral adrenal enlargements (right, 5 cm; left 5.5 cm). Both adrenal glands have an amorphous shape and nodular enhancement of the peripheral portion after contrast scan. An approximately 3 cm sized simple cyst with a well-defined low attenuation is also noted at the anterolateral aspect of the left kidney.
3 ADRENAL TUBERCULOSIS SIMULATING BILATERAL MACRONODULAR HYPERPLASIA 221 Fig. 2. MRI of the pituitary gland. An approximately cm sized less enhancing nodule is noted at the Rt. pituitary gland. The pituitary stalk is displaced to the Lt. side as a result of this mass. Another tiny cystic nodule is noted at the central portion of the pituitary gland, immediately posterior to the stalk insertion site. Fig. 3. Microscopic findings of the left adrenal gland show a chronic granulomatous inflammation with central necrosis and multinucleated giant cells, suggesting a mycobacterial infection. ing pituitary adenoma as the cause of her Cushing s syndrome. The basal central to peripheral ACTH ratio was 4.52 and the post-crh stimulation ratio was 4.25, indicating the existence of an ACTH producing pituitary tumor (Table 1). Therefore, she underwent a transsphenoidal adenomectomy (TSA) and an immunohistochemical study using anti-acth antibodies positively stained the cytoplasm in most of the adenoma cells. After surgery, the plasma ACTH and serum cortisol levels decreased to pg/ml and 1.3 g/dl, respectively. Five months after TSA, she complained of severe pain in both flanks, and a follow-up abdominal CT was performed. Both adrenal glands were enlarged (right 6 cm, left 7 cm) compared with that of before the TSA. Plasma ACTH levels were pg/ml in the early morning and pg/ml in the evening, and Serum cortisol levels were g/dl in the early morning and 8.22 g/dl in the evening. Level of urinary free cortisol excretion was 5.22 g/day (normal range; 0 77). A hormonal study showed no evidence of a recurrence of the hypercortisolism or adrenal autonomy. Given the malignant potential and pressure symptoms of the adrenal mass as a result of the rapidly increasing size and intractable flank pain, a left adrenalectomy was performed. The left adrenal gland measured cm and weighed 110 g. A macroscopic examination showed that the gland had a pale brown ragged external surface, and showed a pale gray, greasy and yellow necrotic cut surface on sectioning. Microscopically, chronic granulomatous inflammation with central necrosis and multinucleated giant cells was observed, which suggested a mycobacterial infection (Fig. 3). Therefore, her tuberculosis medication was changed to a secondary regimen. After changing her medication, the right adrenal mass measuring 5 4 cm decreased in size to 4 3 cm. One year after the adrenalectomy, she showed no clinical evidence of Cushing s disease, and her 24-h urinary free cortisol level was normal at 48.7 g/day and her early morning cortisol level was g/dl. Rapid ACTH stimulation test showed adequate cortisol response (20 g/dl). After that, she discontinued steroid replacement therapy and until now she has taken no replacements for glucocorticoids or mineralocorticoids. Discussion This paper presented a case of Cushing s disease with bilateral adrenal enlargement, which was once diagnosed as MNH, but was later confirmed to be adrenal tuberculosis by the pathological findings after adrenalectomy. It is often difficult to determine the appropriate treatment option in bilateral adrenocortical hyperplasia, particularly the macronodular form in patients with Cushing s disease, because adrenal hyperplasia be-
4 222 KWON et al. come autonomous. In that case, most patients require an adrenalectomy as well as the removal of the functional pituitary mass. In our patient, it was believed that the bilateral MNH was the result of long standing ACTH stimulation from the pituitary adenoma. The first choice treatment for Cushing s disease is surgical removal of the pituitary mass. Therefore, it was expected that bilateral adrenal enlargements would regress after pituitary surgery. Some cases in which the adrenal tumors regressed following pituitary surgery have been reported [5 7]. However, five months after trans-sphenoidal surgery, even though the pituitary macroadenoma had been successfully removed, the adrenal mass enlarged, and the patient complained of intermittent intractable abdominal pain. A hormonal study revealed that Cushing s disease had been cured, and there was no evidence of hypercortisolism or autonomy of the adrenal gland. As a consequence, it was difficult to decide the next treatment plan because of the obscurity of the adrenal mass. The patient underwent a left adrenalectomy to explore the nature of the rapidly enlarging adrenal mass, and the pathological findings confirmed adrenal tuberculosis. Smals et al. [1] showed that the adrenal weight in the patients with MNH correlates with the duration of the disease, and suggested MNH may be the result of long-standing Cushing s disease with varying degrees of pituitary dependence and adrenocortical autonomy, which can lead to confusing biochemical and radiological findings. The left adrenal gland was so large in our patient (weighing 110 g) that it suggested a long duration of the disease and chronic stimulation by ACTH. Some cases of Cushing s syndrome have been reported that show a transition from pituitary dependency to autonomy of the adrenal gland [8]. Sturrock et al. [9] reported a patient with a serum ACTH that was initially 31 ng/l but became undetectable during the course of investigation. The trans-sphenoidal removal of a corticotroph adenoma did not affect the serum cortisol level and she underwent a unilateral adrenalectomy for the adrenal adenoma. When the serum cortisol is not suppressed by high dexamethasone doses, a differential diagnosis from other causes such as Cushing s syndrome caused by MNH becomes quite important for surgical treatment. Usually the plasma ACTH level in the case of Cushing s disease is slightly higher than the normal range. On the other hand, in the case of Cushing s syndrome, it is lower than the normal value due to the autonomic adrenocortical nodular hyperplasia as a result of a negative feedback phenomenon. In our patient, the first choice of treatment was based on the increased ACTH levels and pituitary secretion of the ACTH from the inferior petrosal sinus sampling. Nodular hyperplasia may be an intermediary stage between diffuse hyperplasia and the appearance of an autonomous adenoma after the long-term stimulation of the hyperplastic gland. A rare case of Cushing s disease coexisting with a single macronodule simulating the adenoma of the adrenal cortex has been reported [10]. Endocrinologic tests indicated Cushing s disease, whereas the radiological findings suggested a left adrenal adenoma. A left adrenalectomy followed by pituitary irradiation was performed. The patient had spinal tuberculosis with pulmonary involvement. Although the pulmonary lesion was cleared after medication, M. tuberculosis had spread into the adrenal gland hematogenously. It is possible that the hypercortisolism due to Cushing s disease might have reactivated or aggravated the pre-existing tuberculosis. A large volume of experimental data exists concerning the fact that glucocorticoids increase the susceptibility of sensitive subjects to reactivation and dissemination of tuberculosis upon prolonged exposure to pharmacological doses of glucocorticoids. However, the exact mechanism has not been defined. In a review of natural Cushing s syndrome cases [11], infections accounted for approximately one half of the deaths in the autopsied cases with Cushing s syndrome. Nine patients were found to have tuberculosis, which is a similar rate to that found in the general autopsy population. It has been pointed out that although experimental tuberculosis is markedly aggravated by glucocorticoids, its prevalence in humans treated with them is low. Adrenal tuberculosis is a well-known cause of primary adrenal insufficiency. Considering that the urinary excretion of free cortisol in our patient was >4 times the normal level in most Cushing syndrome patients, her 24 hr urine free cortisol level was not that high (90.86 g/day). She had taken anti-tuberculosis medication including rifampin. The major site of cortisol metabolism is the liver and rifampin is a wellknown hepatic enzyme inducer that affects the metabolism of cortisol. According to previous reports about the effect of rifampin on cortisol metabolism, rifampin accelerates the metabolism of cortisol resulting in decrease of urinary free cortisol level without any changes in basal cortisol levels [12]. Actually we did not
5 ADRENAL TUBERCULOSIS SIMULATING BILATERAL MACRONODULAR HYPERPLASIA 223 check hormone levels or do any tests without anti-tbc medication. Inadequate urine collection also might affect the urinary cortisol level. Otherwise, this discrepancy might be due to the coincident mild adrenal insufficiency resulting from the adrenal tuberculosis. It is possible that a primary adrenal insufficiency will develop in future because of the adrenal cortical destruction of the right adrenal gland. However, to date, our patient has showed no evidence of adrenal insufficiency. This might due to some intact area in the adrenal cortex that functions the same as the pathologically proven left adrenal gland. To our knowledge, this is the first case report of Cushing s disease with adrenal tuberculosis simulating bilateral MNH. A patient with Cushing s disease with bilateral nodular hyperplasia and histoplasmosis of both adrenal glands has been reported [4]. However, the diagnosis of adrenal histoplasmosis was only made postoperatively. In conclusion, this paper reports a patient with Cushing s disease with bilateral adrenal nodular enlargements as a result of tuberculosis, which mimicked bilateral MNH. References 1. Smals AG, Pieters GF, van Haelst UJ, Kloppenborg PW (1984) Macronodular adrenocortical hyperplasia in long-standing Cushing s disease. J Clin Endocrinol Metab 58: Tabarin A, Magimel S, Laurent F, Navarranne A, Guerin J, Roger P (1992) Biological and developmental aspects of macronodular adrenal hyperplasia in Cushing s disease. Ann Endocrinol Metab (Paris) 53: Sanford JP, Favour CB (1956) The interrelationships between Addison s disease and active tuberculosis: A review of 125 cases of Addison s disease. Ann Intern Med 45: Tan TT, Choy YW, Norizan MA, Meah F, Khalid BA (1990) Adrenal histoplasmosis in Cushing s syndrome with bilateral adrenocortical nodular hyperplasia. Med J Malaysia 45: Aron DC, Findling JW, Fitzgerald PA, Brooks RM, Fisher FE, Forsham PH, Tyrell JB (1981) Pituitary ACTH dependency of nodular adrenal hyperplasia in Cushing s syndrome. A report of two cases and review of the literature. Am J Med 71: Abs R, Nobels F, Verhelst J, Chanson P, Mahler C, Corthouts B, Blockx P, Beckers A (1993) Hyperfunctioning unilateral adrenal macronodule in three patients with Cushing s disease: Hormonal and imaging characterization. Acta Endocrinol 129: Fish HR, Sobel DO, Miegel CA (1986) Macronodular adrenal hyperplasia with hypothalamic-pituitary-adrenal suppression by ultra-high-dose dexamethasone: regression following hypophysectomy. Clin Neuropharmacol 9: Lopez JM, Sapunar J, Donoso J, Martinez P (1991) Cushing s syndrome due to bilateral adrenal macronodular hyperplasia. From ACTH-dependent hypercortisolism to ACTH-independent hypercortisolism. Revista Medica de Chile 119: Sturrock ND, Morgan L, Jeffcoate WJ (1995) Autonomous nodular hyperplasia of the adrenal cortex: tertiary hypercortisolism. Clin Endocrinol 43: Leiba S, Shindel B, Weinberger I, Fuchs J, Rotenberg Z, Mor C, Kaufman H (1986) Cushing s disease coexisting with a single macronodule simulating adenoma of the adrenal cortex. Acta Endocrinol (Copenh) 112: Plotz CM, Knowlton AI, Ragan C (1952) The natural history of Cushing s syndrome. Am J Med 13: Keven K, Uysal AR, Erdogan G (1998) Adrenal function during tuberculous infection and effects of antituberculosis treatment on endogenous and exogenous steroids. Int J Tuberc Lung Dis 2:
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