Case Report. Pregnancy with Cushing s syndrome is generally rare, but it is common to have a baby
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1 AACE Clinical Case Reports Rapid Electronic Articles in Press Rapid Electronic Articles in Press are preprinted manuscripts that have been reviewed and accepted for publication, but have yet to be edited, typeset and finalized. This version of the manuscript will be replaced with the final, published version after it has been published in the print edition of the journal. The final, published version may differ from this proof. DOI: /ACCR AACE. Case Report A CASE OF ACTH-DEPENDENT CUSHING SYNDROME CAUSED BY THYMIC CARCINOID THAT WAS DIAGNOSED AFTER THE DELIVERY OF A HEALTH CHILD, A CASE REPORT Takeshi Hayashi; Kumi Kobayashi; Azusa Yamato; Daisuke Matsutani; Hanako Ide; Yasushi Kanazawa; Kennosuke Ohashi; Kenji Yamashiro; Katsuyoshi Tojo; Masaya Sakamoto; Kazunori Utsunomiya From: The Jikei University School of Medicine Division of Diabetes, Metabolism and Endocrinology, Department of Internal Medicine; Tokyo, Japan Abstract Object Pregnancy with Cushing s syndrome is generally rare, but it is common to have a baby with Cushing's syndrome. However there has been no report of an ACTH-producing carcinoid diagnosed promptly after delivery. We present the first report of a woman with untreated Cushing s syndrome caused by an ACTH-producing thymic carcinoid who gave birth to a healthy child. Methods A 21-year-old female underwent a caesarean section because of rupture of membranes 1
2 at 31 weeks of pregnancy. Two months after delivery, she was aware of pedal edema, and it worsened rapidly. Two more weeks later, she visited our hospital. Results Endocrinological examination revealed high levels of ACTH (527 pg/ml) and cortisol (113 μg/dl) that were not affected by overnight dexamethasone (DEX) suppression tests. Subsequently performed chest and abdominal dynamic computed tomography (CT) showed a huge mediastinal tumor (3.8 cm in diameter) and enlargement of the adrenal glands. Aided by the results of immunohistochemistry from a biopsy specimen, we made the diagnosis of ectopic ACTH-dependent Cushing s syndrome, following which a tumorectomy was performed. The tumor was finally diagnosed as an atypical thymic carcinoid with positivity for synaptophysin, chromogranin A, and ACTH. Conclusion We present the first report of a woman with untreated Cushing s syndrome caused by an ACTH-producing thymic carcinoid who gave birth to a healthy child. Key words ectopic ACTH syndrome, thymic carcinoid, pregnancy. Abbreviations: 2
3 Na = sodium, K = potassium, Cl = Chlorine, Ca = calcium, P = phosphorus, PG = plasma glucose, HbA1c = Hemoglobin A1c, TSH = thyroid-stimulating hormone, FT3 = free triiodothyronine, FT4 = free thyroxine, GH = growth hormone, IGF-I = insulin-like growth factor I, LH = luteinizing hormone, FSH = follicle stimulation hormone, PRL = prolactin, ACTH = adrenocorticotropic hormone, DHEA-S = dehydroepiandrosterone sulfate, PRA = plasma renin activity, PAC = plasma aldosterone concentration; CT = computed tomography. DEX = dexamethasone; CRH = corticotropin-releasing hormone; MRI = magnetic resonance imaging, HPF = high power field; CD = cluster of differentiation; UFC = urinary free cortisol; NICU = neonatal intensive care unit; POMC = pro-opiome lanocortin. Introduction In Cushing s syndrome, rare menstruation or amenorrhea occurs with high frequency because pituitary gonadotropins are suppressed by excessive glucocorticoids. Therefore pregnancy in women with Cushing s syndrome is generally rare, and it is extremely rare to deliver a baby without a prior diagnosis of Cushing s syndrome. There are over 140 reported cases of Cushing s syndrome in pregnancy. However, only 6 reports describe ectopic ACTH syndrome, and there is no report of an ACTH-producing carcinoid in a patient not under treatment of Cushing s syndrome delivering a healthy child (1-6). We herein report such a patient who was diagnosed with an ACTHproducing thymic carcinoid promptly after delivering a healthy child. Case report The patient is a 21-year-old female of Dravidian origin without any noteworthy personal or family history. Before pregnancy, her body weight was 48 kg. But it 3
4 increased to 60.7 kg at the 24 th and 64 kg at the 28 th week of pregnancy. Blood pressure had been around 120/70 mmhg. Blood glucose during the pregnancy was around 120 mg/dl, although the patient did not undergo a 75g oral glucose tolerance test. At 31 weeks into the pregnancy, a caesarean section was performed due to rupture of membranes. At this stage, the cause of the premature birth was not specifically determined. The patient visited our hospital two more months after delivery due to significant pedal edema. Physical examination revealed pitting edema and a typical cushingoid appearance including a moon face, acne vulgaris, hirsutism, central obesity, and a buffalo hump. HbA1c increased to 9.4%, and serum potassium is as low as 2.5 mmol/l (Table 1). Endocrinological examination revealed high levels of ACTH (527 pg/ml) and cortisol (113 μg/dl). The patient was hospitalized immediately and with urgency. Her height was cm, body weight was 64 kg, and body mass index was 28.4 kg/m 2. Blood pressure was 150/100 mmhg and heart rate was 60 beats per minute and regular. Chest and abdominal dynamic CT showed a huge mediastinal tumor (3.8 cm in diameter) and enlargement of the adrenal glands (Figure 1A, B). The tumor on the chest X-ray of the day after delivery was found which was not pointed out at that time. Hormonal evaluation revealed the absence of a circadian rhythm of production of ACTH and cortisol. Cortisol levels were not suppressed by administration of 0.5 mg and 8 mg dexamethasone (DEX). A CRH stimulation test showed that both ACTH and cortisol levels were high, and that there was no response to CRH (Table 2). No pituitary 4
5 adenoma was observed using magnetic resonance imaging (MRI). Based on the above, we suspected ectopic ACTH syndrome due to the presence of a mediastinal tumor and performed a needle biopsy. Immunohistochemistry of the tumor showed positivity for synaptophysin, chromogranin A, and ACTH. As a result, we diagnosed an ACTHproducing thymic carcinoid. Thymic carcinoid may be associated with multiple endocrine neoplasia type 1 (MEN1) syndrome in <5% of patients. The European Neuroendocrine Tumor Society (ENETS) recommends screening for MEN1 (7). In the present case, the ionized calcium and PTH level were normal and swelling of the parathyroid gland was not clear from the ultrasonic examination. There is no family history of MEN-1. Although there is a possibility of an orphan, we did not find other symptoms enough to perform genetic testing. In such cases, it is also crucial to determine the presence of distant metastases. The most common sites of metastases are the liver, bones, and mediastinal lymph nodes (8). From the chest and abdominal dynamic CT, we did not recognize metastases to the liver and mediastinal lymph nodes. In the lumbar spine MRI, bone metastases were not observed. The patient was treated with insulin injections, oral potassium, and metyrapone (750 mg/day). ACTH and cortisol levels went down immediately. Finally, a tumorectomy was performed under oral administration of metyrapone (1500 mg/day) and hydrocortisone (30 mg/day) (Figure 2). Blood pressure was good control without antihypertensive drug. Macroscopic findings indicated that the carcinoid tumor measured cm and had not 5
6 expanded outside the thymus. Examination of the needle biopsy of the mediastinal mass showed restiform, ribbony, alveolar cells that contained round, spindle, multinuclear nuclei. Immunohistochemistry of tumor cells showed positivity for synaptophysin, CD56, and chromogranin A, and there were both necrosis and mitoses of 5/10 HPFs (Figure 1C-F). Based on the above, the tumor was diagnosed as an atypical carcinoid as classified by the World Health Organization. Also, immunohistochemical analysis showed positive staining of tumor cells for ACTH. According to ENETS, there is no consensus on adjuvant therapy for pulmonary carcinoids after complete resection. In the present case, we thought the tumor was resected completely because pleural invasion was not observed. Therefore, we administered no medical therapy after surgery. Twelve months after the surgery, she takes oral hydrocortisone (10 mg per day). The patient is in good clinical condition, and the disease is stable without any rise in ACTH and cortisol. Nor is there any evidence of local or systemic progression. Discussion We diagnosed the patient as having ectopic ACTH syndrome due to the ACTHproducing thymic carcinoid. Although Cushing s syndrome is common among women of childbearing age, the occurrence of pregnancy is generally considered as rare. The reason for the infertility is due to suppression of pituitary gonadotropin by excessive 6
7 glucocorticoid causing a decline in the follicle-endometrium. Amenorrhea and oligomenorrhea were observed in 70-80% of cases (9). Therefore, patients with Cushing s syndrome who become pregnant without treatment are extremely rare. It is difficult to diagnose Cushing s syndrome during pregnancy because the clinical features of Cushing s syndrome overlap with mental and physical signs that occur in pregnant women without Cushing s syndrome. Increased hypothalamic-pituitary-adrenal axis activity, including increases in urinary free cortisol (UFC), cortisol-binding globulin, and total plasma cortisol, can also be seen during normal pregnancy. The use of latenight salivary cortisol is recommended for diagnosis. It was reported that Cushing s syndrome during pregnancy can be diagnosed when the UFC is more than four times the upper limit of that in the non-pregnant state or when salivary cortisol is two to three times above the upper limit of normal (10) (11). If women with Cushing s syndrome become pregnant, maternal complications commonly occur: hypertension (60-80%), glucose tolerance disorder (15-25%), toxemia of pregnancy (14%), heart failure (3%), and psychiatric disorders (4%) (12). In the present case, high blood pressure during pregnancy was not evident. Blood glucose level was slightly elevated, (approximately 120 mg/dl in the late pregnancy). Although the patient did not undergo a 75g oral glucose tolerance test, she was considered to have been diabetic since late pregnancy at least from the result of HbA1c after two months delivery. There are other influences of Cushing s syndrome on pregnancy: fetal complications, 7
8 preterm birth (60%), neonatal mortality (1.5-20%), and intrauterine fetal growth failure (15%) (13). However, a fetus with adrenal insufficiency is rare. The fetus is partially protected from hypercortisolemia because placental 11-beta-hydroxysteroid dehydrogenase converts 85% of maternal cortisol to biologically inactive cortisone (2). As to treatment of Cushing s syndrome in pregnancy, tumorectomy at weeks is recommended (1). Indeed, live birth rates appeared to be slightly better in women who received early treatment compared to those who were managed conservatively (1). In the present case, the baby was placed under NICU management because of premature delivery, but its course of growth was good. Regarding drug therapy, metyrapone is most frequently recommended although no drug has been confirmed as sufficiently safe for pregnant women and a fetus (14). In the present case, the patient was administered metyrapone before the carcinoid was excised. Interestingly, both cortisol and ACTH levels decreased. This paradoxical reduction in ACTH could be explained by the fact that the glucocorticoid-dependent POMC positive-feedback loop was canceled by cortisol reduction (15). In fact, ACTH secretion in response to dexamethasone was observed (table 2). In the past, approximately 140 cases of Cushing s syndrome occurring simultaneously with pregnancy were reported but only 6 reports showed ectopic ACTH-producing tumors. To summarize the observations in these 6 cases, 5 had hypertension, 4 had toxemia of pregnancy, 2 had diabetes, one had acute psychosis and one patient died. As 8
9 to fetal complications, preterm birth occurred in 5 cases and stillbirth in one. Carcinoid is classified as a well-differentiated neuroendocrine carcinoma, but often exhibits a clinical picture of malignant invasion, metastasis, and recurrence. Invasion into the surrounding organs was reported in almost 70% of cases (16). Of ectopic ACTHproducing tumors 15 to 40% were carcinoid. However, in surgical cases, where thymic carcinoid was resected at the rate of 87.5%, postoperative recurrence was at a higher rate than for thymic carcinoma. The 5-year survival rate was shown to be 50% in typical carcinoid and 20% in atypical carcinoid (17). Therefore, following surgery, a thorough 10-year follow-up is recommended (18). Finally, we consider the time of onset of the carcinoid. Whether or not the tumor was present before pregnancy in this case is unknown because no chest X-ray images, no examination data before and during the pregnancy were available. Only one day following delivery, an image of a tumor was observed on chest X-ray but we have no information on how long the tumor was present during the pregnancy (Figure 1G). In the present case, from the fact that she did not measure blood pressure at home and no hypertension was seen in hospitalization data at delivery, there was no clear evidence of complications related to hypertension. For this reason, we consider the possibility that the tumor may have been reduced during pregnancy. In fact, comparison of chest X-rays taken the day following delivery with those 80 days after the delivery show expansion of the tumor (Figure 1G, H). 9
10 Conclusion This is the first report of a woman with Cushing s syndrome with an ACTH-producing thymic carcinoid which was diagnosed promptly after delivery of a healthy child. Abbreviations Na: sodium, K: potassium, Cl: Chlorine, Ca: calcium, P: phosphorus, PG: plasma glucose, HbA1c: Hemoglobin A1c, TSH: thyroid-stimulating hormone, FT3: free triiodothyronine, FT4: free thyroxine, GH: growth hormone, IGF-I: insulin-like growth factor I, LH: luteinizing hormone, FSH: follicle stimulation hormone, PRL: prolactin, ACTH: adrenocorticotropic hormone, DHEA-S: dehydroepiandrosterone sulfate, PRA: plasma renin activity, PAC: plasma aldosterone concentration. CT; computed tomography. DEX; dexamethasone. CRH; corticotropin-releasing hormone. MRI; magnetic resonance imaging, HPF; high power field. CD; cluster of differentiation. UFC; urinary free cortisol. NICU; neonatal intensive care unit. POMC; proopiomelanocortin. Declarations Acknowledgements Not applicable. 10
11 Funding Not applicable. Availability of data and materials Not applicable. Authors Contributions KK, AY, DM, HI, YK treated the patient and KK drafted the article. TH, KO, KY, KT, KU and especially MS reviewed and edited the intellectual content. All authors gave final approval for this version to be published. The funder had no role in writing of the manuscript, and the decision to submit the manuscript for publication. Competing interests MS has participated in speaker s bureaus/advisory panels for Sanofi, Daiichi-Sankyo, Astellas, and Tanabe-Mitsubishi. KU has received research support from Terumo, Kowa, Taisho, Arkray, Kyowa Kirin, MSD, Astellas, Boehringer Ingelheim, Ono, Novo Nordisk, Kissei and Tanabe-Mitsubishi and has participated in speaker's bureau/advisory panels for Astellas, Astra Zeneca, Kowa, MSD, Eli Lilly, Taisho, Novo Nordisk and Sanofi. The other authors have no conflict of interest to declare. These 11
12 declared interests do not alter the authors adherence to the policies of AACE Clinical Case Reports on sharing data and materials. Consent for publication Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor of this journal. Ethics approval and consent to participate Not applicable. References 1. Aron DC, Schnall AM, Sheeler LR. Cushing's syndrome and pregnancy. Am J Obstet Gynecol. 1990;162: Guilhaume B, Sanson ML, Billaud L, et al. Cushing's syndrome and pregnancy: aetiologies and prognosis in twenty-two patients. Eur J Med. 1992;1: Hadden DR. Adrenal disorders of pregnancy. Endocrinol Metab Clin North Am. 1995;24: Cohade C, Broussaud S, Louiset E, et al. Ectopic Cushing's syndrome due to a pheochromocytoma: a new case in the post-partum and review of literature. Gynecol 12
13 Endocrinol. 2009;25: Oh HC, Koh JM, Kim MS, et al. A case of ACTH-producing pheochromocytoma associated with pregnancy. Endocr J. 2003;50: Tjalma WA. Successful Pregnancies after the Treatment of a Thymic Carcinoid. Case Rep Obstet Gynecol. volume 2015; Article ID :3 pages M.E.Caplin, E.Baudin, P.Ferolla, et al. Pulmonary neuroendocrine (carcinoid) tumors: European Neuroendocrine Tumor Society expert consensus and recommendations for best practice for typical and atypical pulmonary carcinoids. Annals of Oncology. 2015:26: Bhosale P, Shah A, Wei W, et al. Carcinoid tumours; predicting the lication of the primary neoplasm based on the sites of metastases. Eur Radiol. 2013;23: Pickard J, Jochen AL, Sadur CN, et al. Cushing's syndrome in pregnancy. Obstet Gynecol Surv. 1990;45: Manetti L, Rossi G, Grasso L, et al. Usefulness of salivary cortisol in the diagnosis of hypercortisolism: comparison with serum and urinary cortisol. Eur J Endocrinol. 2013;168: Jung C, Ho JT, Torpy DJ, et al. A longitudinal study of plasma and urinary cortisol in pregnancy and postpartum. J Clin Endocrinol Metab. 2011;96: Lindsay JR, Jonklaas J, Oldfield EH, et al. Cushing's syndrome during pregnancy: 13
14 personal experience and review of the literature. J Clin Endocrinol Metab. 2005;90: Bednarek-Tupikowska G, Kubicka E, Sicinska-Werner T, et al. A case of Cushing's syndrome in pregnancy. Endokrynol Pol. 2011;62: Buescher MA, McClamrock HD, Adashi EY. Cushing syndrome in pregnancy. Obstet Genecol. 1992;79: Sakuma I, Higuchi S, Fujimoto M, et al. Cushing Syndrome Due to ACTH-Secreting Pheochromocytoma, Aggravated by Glucocorticoid-Driven Positive-Feedback Loop. J Clin Endocrinol Metab. 2016;101: Soga J, Yakuwa Y, Osaka M. Evaluation of 342 cases of mediastinal/thymic carcinoids collected from literature: a comparative study between typical carcinoids and atypical varieties. Ann Thorac Cardiovasc Surg. 1999;5: Moran CA, Suster S. Thymic neuroendocrine carcinomas with combined features ranging from well-differentiated (carcinoid) to small cell carcinoma. A clinicopathologic and immunohistochemical study of 11 cases. Am J Clin Pathol. 2000;113: Oberg K, Jelic S. Neuroendocrine bronchial and thymic tumors; ESMO clinical recommendation for diagnosis, treatment and follow-up. Ann Oncol. 2008:19 Suppl2: Table Titles and legends Table1. Laboratory Findings 80 days after delivery of a healthy infant 14
15 Na 143 mmol/l P 4.1 mmol/l K 2.5 mmol/l PG 866 mg/dl Cl 92 mmol/l HbA1c 9.4% Ca 9.2 mg/dl TSH 0.36 μiu/ml ACTH 527 pg/ml FT pg/ml Cortisol 113 μg/dl FT4 1.3 ng/dl DHEA-S 313 μg/ml GH 0.13 ng/ml PRA 0.3 ng/ml/min IGF-1 87 ng/ml PAC 166 pg/ml LH 0.11 mlu/ml Urinary free cortisol (24hr) 4950 μg/day FSH 1.09 mlu/ml Urinary free aldosterone (24hr) 4.0 μg/day PRL 4.57 ng/ml Legend: Blood glucose and HbA1c values were high and hypokalemia was present. Table2. Diurnal variation of plasma ACTH and cortisol levels, Dexamethasone suppression test and CRH stimulation test Diurnal variation of plasma ACTH, cortisol levels 8:00 16:00 23:00 ACTH (pg/ml) Cortisol (µg/dl) Dexamethasone suppression test 0.5 mg 8 mg ACTH (pg/ml) Cortisol (µg/dl) CRH stimulation test before 30 min 60 min 90 min 120 min ACTH (pg/ml) Cortisol (µg/dl) Legend: Hormonal evaluation revealed the absence of a circadian rhythm of ACTH and cortisol caused by elevation of ACTH. Cortisol levels were not suppressed by administration of 0.5 mg and 8 mg DEX. In CRH stimulation test, both ACTH and cortisol values were high during the test, and there was no response to CRH. 15
16 Figure Titles and legends Figure 1. Chest and abdominal dynamic computed tomography. Macroscopic findings, pathology. Chest X-ray. Legend: Chest and abdominal dynamic computed tomography shows a huge mediastinal tumor (3.8 cm in diameter) and enlargement of the adrenal glands (A,B). Carcinoid tumor measured cm, and macroscopic findings showed that it had not expanded outside the thymus (C). Immunohistochemistry of the tumor showed positivity for synaptophysin (D), Chromogranin A (E) and ACTH (F). Day following delivery the mediastinal tumor was observed (G). Eighty days after delivery the tumor had expanded (H). Figure 2. Change in ACTH and cortisol values Legend: The patient was treated with metyrapone (750 mg/day). ACTH and cortisol levels went down immediately. Finally, a tumorectomy was performed under oral administration of metyrapone (1500 mg/day) and hydrocortisone (30 mg/day). Twelve months following surgery, the patient takes oral hydrocortisone (10 mg/day). The patient is in good clinical condition, the disease is stable without a rise in ACTH and cortisol, nor any evidence of local or systemic progression. 16
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