CATATONIA INDUCED BY AN ACTH-SECRETING NEUROENDOCRINE TUMOR: A CASE REPORT
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1 Case Report CATATONIA INDUCED BY AN ACTH-SECRETING NEUROENDOCRINE TUMOR: A CASE REPORT Tien Sy Dong, MD*; Jonathan Thompson Henry, PhD*; Katherine Stanley, MD; Silvana Pannain, MD ABSTRACT Objective: The catatonic reaction is a striking syndrome associated with a variety of psychiatric and medical conditions, including high-dose corticosteroid therapy. We present the case of a patient who suffered increasing mental disturbance to the point of catatonia in the setting of an adrenocorticotropic hormone (ACTH)-secreting neuroendocrine tumor and severe hypercortisolism. We describe the presentation and course of treatment with benzodiazepines and pancreaticoduodenectomy. Methods: A PubMed literature search was done to summarize and compare this case to other reported cases of psychiatric disturbances in the setting of hypercortisolism. Results: Our literature review of case reports from noted 7 cases of catatonic reactions to glucocorticoid or ACTH administration. We hypothesize that the catatonia in our patient was caused by elevated levels of cortisol secondary to ectopic ACTH overproduction, making this report the first documented case of catatonia secondary to an ACTH-secreting neuroendocrine tumor. Conclusion: Catatonia is a rare clinical presentation of an ACTH-secreting neuroendocrine tumor, which can be successfully controlled with benzodiazepines and definitively treated with pancreaticoduodenectomy. (AACE Clinical Case Rep. 2015;1:e245-e249) Submitted for publication September 17, 2014 Accepted for publication January 12, 2015 *These authors contributed equally to the writing of the manuscript. From the Department of Medicine, University of Chicago, Chicago, Illinois. Address correspondence to Dr. Tien Dong; Department of Medicine, University of Chicago, 5841 South Maryland Avenue, MC 3051, Chicago, IL tien.dong@uchospitals.edu. DOI: /EP14431.CR To purchase reprints of this article, please visit: Copyright 2015 AACE. Abbreviations: ACTH = adrenocorticotropic hormone; CT = computed tomography; ECT = electroconvulsive therapy; NMDA = N-methyl-D-aspartate; POD = postoperative day INTRODUCTION Although catatonia has been historically described as a subtype of schizophrenia and major mood disorder (1), it is now understood to be associated with a variety of psychiatric illnesses as well as general medical conditions. The key feature of catatonia is the inability of the patient to move normally despite having the physical capacity to do so (1). The most common manifestations are immobility (hypokinesis or akinesis), mutism, negativism (defined as resistance to instructions to move or maintenance of a rigid posture against attempts to be moved), staring, posturing, and withdrawal. Other signs include purposeless movement, waxy flexibility, and echophenomena (2). The prompt diagnosis of catatonia is important, as antipsychotic medications may actually worsen the patient s symptoms (3). There are 3 major categories of catatonia: retarded, excited, and malignant (4). Retarded catatonia is characterized by mutism, negativism, posturing, and hypokinesis/ akinesis. In contrast, excited catatonia is marked by excessive purposeless movements and restlessness. Unlike the other 2 categories, malignant catatonia is a life-threatening condition that has several features that overlap with neuroleptic malignant syndrome: fever, autonomic instability, delirium, and rigidity. The treatment of catatonia should target the underlying condition if at all possible, but the mainstay of treatment often includes the use of benzodiazepines and in severe cases electroconvulsive therapy (ECT) (1). As catatonia has been associated with many AACE CLINICAL CASE REPORTS Vol 1 No. 4 Autumn 2015 e245
2 e246 ACTH-Secreting NETs, AACE Clinical Case Rep. 2015;1(No. 4) general medical conditions, finding the underlying cause may be challenging. One precipitant of catatonia is exogenous or endogenous corticosteroid excess; the literature contains several cases of catatonia secondary to corticosteroid or adrenocorticotropic hormone (ACTH) administration (5-10), as well as 1 case of catatonia secondary to a cortisol-secreting adrenal carcinoma (11). We present a case of catatonia caused by an ACTH-secreting neuroendocrine tumor. CASE REPORT The patient is a 45-year-old female with a history of hypothyroidism who presented to her primary care doctor with 3 weeks of swelling of her face, abdomen, and legs. Over the prior 6 months, she had developed worsening psychiatric and cognitive symptoms. Psychiatric symptoms included irritability, sad affect, decreased motivation, and social withdrawal, and signs of cognitive dysfunction included difficulties with her usual activities such as paying bills, shopping, cooking, and driving. She additionally noted 20 pounds of unintentional weight loss and easy bruising. Her physical exam was notable for a Cushingoid appearance: round face, erythematous reticular rash on her chest, purple abdominal striae, and lower extremity swelling. Initial laboratory tests showed hypokalemia, alkalosis, and hyperglycemia. A random serum ACTH level was 348 pg/ml (normal, <52 pg/ml), and a random cortisol level was 145 µg/dl. Because of the high level of ACTH, her Cushing syndrome was thought to be ACTH-dependent and most likely ectopic. A pituitary magnetic resonance imaging (MRI) scan did not show any pituitary abnormalities. A computed tomography (CT) scan of her abdomen revealed 3 homogenously enhancing soft-tissue masses arising from the serosal surface of the duodenum, with retroperitoneal lymphadenopathy and bilateral enlarged adrenal glands (Fig. 1). She was subsequently admitted, and a fine-needle aspirate (FNA) of a retroperitoneal lymph node was consistent with a low-grade neuroendocrine tumor. Further laboratory findings included a 24-hour urine cortisol of 3,520 µg, carcinoembryonic antigen of 1.7 ng/ml (normal, <5 ng/ml), cancer antigen 125 of 10 U/mL (normal, <35 U/ ml), cancer antigen 19-9 of 11 U/mL (normal, <37 U/ ml), and chromogranin A of 8.6 ng/ml (normal, <93 ng/ ml). Her hypokalemia and alkalosis persisted throughout her initial hospitalization, with a potassium range of 2.5 to 3.1 meq/l despite daily repletion and bicarbonate of 29 to 31 meq/l. This is consistent with prior cases where cortisol may act as a mineralocorticoid when in excess, perhaps by saturating the 11-beta-hydroxysteroid-dehydrogenase enzyme, which inactivates cortisol at the renal tubule (12). A fluorodeoxyglucose positron emission tomography scan was done for staging, and it showed hypermetabolic activity in the area of the abdominal masses and bilateral adrenal hyperplasia, with no other areas of uptake. She was given a stage of T2N1M0. Bilateral inferior petrosal sinus sampling was deferred because her laboratory findings, imaging, and FNA biopsy were most consistent with her having Cushing syndrome from an ectopic ACTH-secreting neuroendocrine tumor. A plan was made to attempt operative resection of these masses, and she was started on ketoconazole to lower her cortisol levels until the procedure. Fig. 1. Sagittal and coronal views of initial computed tomography scans of the abdomen and pelvis. Imaging shows 3 homogenously enhancing soft-tissue masses arising from the serosal surface of the duodenum. The largest of the masses measures mm.
3 ACTH-Secreting NETs, AACE Clinical Case Rep. 2015;1(No. 4) e247 On hospital day 4, the patient became nonverbal. She was akinetic, with a rigid posture in bed and resisted passive movement. Pupils and reflexes were normal. Head CT, electroencephalography (EEG), lumbar puncture, and metabolic and infectious work-up all showed no major abnormalities, and a paraneoplastic panel and anti Nmethyl-D-aspartate (NMDA)-receptor antibody titer were obtained, which later returned normal. She was given a trial dose of intravenous (IV) lorazepam 1 mg, with almost immediate improvement in her motor function and mental status. She had continued improvement with scheduled dosing of lorazepam, though she remained moderately confused and minimally verbal. She was diagnosed with retarded catatonia, most likely due to a general medical condition, suspected to be hypercortisolism secondary to an ACTH-secreting neuroendocrine tumor. On hospital day 15, the patient underwent resection of her abdominal masses, which included a Whipple procedure (pancreaticoduodenectomy). Her postoperative course was complicated by hypotension, lactic acidosis, and coagulopathy resulting in hemorrhage requiring reoperation. She was treated with high-dose hydrocortisone 100 mg IV every 6 hours, as she was presumed to be adrenally insufficient after removal of the tumors. She was sufficiently stable to be extubated on postoperative day (POD) 2. After extubation, she was noted to have recurrence of symptoms similar to those experienced pre-operatively, including mutism, rigidity, hypokinesis, posturing, and stereotyped writing of nonsensical characters in a notebook. She again responded to benzodiazepine treatment, with some improvement in her mental status and motor function. Her hydrocortisone dose was decreased as her medical condition continued to improve, and her ACTH level decreased from 870 pg/ml pre-operatively to <5.0 pg/ml on POD 2. Her mental status continued to improve as the hydrocortisone dose was decreased. A corticotropinreleasing hormone stimulation test was performed on POD 13 and showed a rise in cortisol from a baseline of 19.8 µg/dl to a peak of 34.5 µg/dl at 30 minutes and a rise in ACTH from 9.7 pg/ml at baseline to a peak of 43.9 pg/ml at 30 minutes. These results were consistent with recovery of her hypothalamus-pituitary-adrenal axis; therefore, the hydrocortisone was stopped completely. She was then discharged to rehabilitation on a lorazepam taper, and her mental status normalized. Pathologic analysis of the surgical specimens revealed 4 well-differentiated low-grade neuroendocrine neoplasms: 4.4-cm paracaval, 5.5-cm uncinate, 2.9-cm peripancreatic, and 1.5-cm ampullary. Immunohistochemistry staining for ACTH was negative, which after a discussion with our pathology department, was found not to be uncommon given the type of antibodies that are utilized within our institution. She has done well since discharge, with no evidence of recurrence and no further psychiatric symptoms. DISCUSSION Psychiatric disturbance following exogenous ACTH or steroid administration was noted in the medical literature soon after pituitary ACTH and cortisone became clinically available in the mid-twentieth century (5,13); these reactions ranged from mild elation to frank psychosis and were observed in up to 18% of patients receiving greater than 80 mg of prednisone per day (14). Our literature review of case reports from noted 7 cases of catatonic reactions to glucocorticoid or ACTH administration (Table 1). The age of onset was between 11 and 62 years; the duration of steroid use ranged from 10 days to 6 months; the doses were equivalent to at least 40 mg of prednisone per day (5-10), with the exception of case 6, who received the equivalent of 26 mg of prednisone per day but had also received ACTH prior, reportedly without psychiatric symptoms, and case 7, who received ACTH only (6). Once the cause of catatonia was identified and the offending agents were tapered, motor symptoms for these patients generally resolved, though mental status sometimes took months to return to normal (case 3 also required ECT). We hypothesize that the catatonia in our patient was caused by elevated levels of cortisol secondary to ectopic ACTH overproduction, making this report the first documented case of catatonia secondary to an ACTH-secreting neuroendocrine tumor. Although it is not uncommon for patients with endogenous Cushing syndrome to present with psychiatric illness, catatonia is a rare presentation. In a case series of 209 patients with Cushing syndrome, 65% of patients had some form of psychiatric abnormality during their illness, including affective symptoms, confusion, and hallucination (15). These findings are further corroborated by a longitudinal study of 30 patients with Cushing syndrome, in which 25 (83%) of the patients met diagnostic criteria for an episode of affective disorder during the course of their illness (16). One previous case of catatonia has been reported in a patient with Cushing syndrome due to a cortisol-secreting adrenal carcinoma (11). Her catatonia initially resolved after the tumor was removed, but she experienced episodes of mild catatonic symptoms upon the eventual relapse of her cancer. The neurobiology of catatonia remains poorly understood. Due to ethical and practical concerns, functional neuroimaging studies have focused on catatonic patients many days after acute presentation and treatment (17,18). These patients have been found to have lingering deficits in the medial motor loop, which includes the supplementary motor area, thalamus, and basal ganglia, consistent with impairment in self-initiated movements (18). Such patients were also found to have altered functionality of the orbitofrontal cortex, a brain region involved with emotional processing (17). To our knowledge, the pathway by which
4 e248 ACTH-Secreting NETs, AACE Clinical Case Rep. 2015;1(No. 4) Table 1 Literature Case Reports of Steroid-Related Catatonia Published Between 1952 and 2011 Case number Patient information Maximum dose/level Citation year-old F with cortisolproducing adrenal carcinoma 20-year-old F abusing steroids for weight gain 3 17-year-old M with colitis year-old F with multiple myeloma 11-year-old M with suspected dermatomyositis 6 41-year-old F with lymphoma year-old M with osteitis deformans 62-year-old F with rheumatoid arthritis Plasma cortisol 686 mmol/l Steinberg, 1996 (11) Dexamethasone 8 mg qd PO Dada et al, 2011 (10) Hydrocortisone 100 mg IV qid, ACTH 40 units IM qd Doherty et al, 1991 (9) Prednisone 60 mg qd PO Grigg, 1989 (8) Prednisone 50 mg qd PO Cortisone 1,300 mg over 10 days (130 mg qd), previous course of ACTH 2,565 mg over 30 days ACTH 1,040 mg given over 12 days Total of cortisone 2,775 mg IM in 2 doses 12 days apart (average of 213 mg per day) Sullivan and Dickerman, 1979 (7) Clark et al, 1953 (6) Clark et al, 1953 (6) Clark et al, 1952 (5) Abbreviations: ACTH = adrenocorticotropic hormone; F = female; IM = intramuscular; IV = intravenous; PO = orally; qid = 4 times a day; qd = every day. corticosteroids promote catatonia is even more opaque. Whether produced in excess or administered exogenously, corticosteroids are known to affect the function of a variety of brain structures, such as the amygdala, the hippocampus, and the frontal lobes and are likely related to more common psychiatric processes such as depression and posttraumatic stress disorder (19). The amygdala, a structure involved in fear and emotional learning, is richly connected to the orbitofrontal cortex (17), though we do not yet know if it plays a role linking corticosteroids, emotional regulation, and motor dysfunction. Future studies are required to shed light on this phenomenon. Other possible causes of catatonia were evaluated in our patient. Catatonia has been reported as a manifestation of paraneoplastic syndrome and anti-nmda encephalitis (20). In our patient, a paraneoplastic panel and anti-nmda antibodies were tested and both were negative. Given her normal EEG, MRI, lumbar puncture, and serologic testing, excess endogenous cortisol secondary to ectopic ACTH production by her neuroendocrine tumors is hypothesized to be the cause of this patient s catatonia. CONCLUSION In summary, high-corticosteroid state is a documented precipitant of catatonic symptomatology; we present a novel case of retarded catatonia caused by an ACTHsecreting tumor. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Fink M, Taylor MA. The catatonia syndrome: forgotten but not gone. Arch Gen Psychiatry. 2009;66: Francis A. Catatonia: diagnosis, classification, and treatment. Curr Psychiatry Rep. 2010;12: Lee JW. Neuroleptic-induced catatonia: clinical presentation, response to benzodiazepines, and relationship to neuroleptic malignant syndrome. J Clin Psychopharmacol. 2010;30: Fink M, Taylor MA. The many varieties of catatonia. Eur Arch Psychiatry Clin Neurosci. 2001;251(suppl 1):I8-I Clark LD, Bauer W, Cobb S. Preliminary observations on mental disturbances occurring in patients under therapy with cortisone and ACTH. N Engl J Med. 1952;246: Clark LD, Quarton GC, Cobb S, Bauer W. Further observations on mental disturbances associated with cortisone and ACTH therapy. N Engl J Med. 1953;249: Sullivan BJ, Dickerman JD. Steroid-associated catatonia: report of a case. Pediatrics. 1979;63: Grigg JR. Prednisone mood disorder with associated catatonia. J Geriatr Psychiatry Neurol. 1989;2: Doherty M, Garstin I, McClelland RJ, Rowlands BJ, Collins BJ. A steroid stupor in a surgical ward. Br J Psychiatry. 1991;158: Dada MU, Oluwole L, Obadeji A, Ajayi OA. Dexamethasone induced psychosis presenting with catatonic features. Afr J Psychiatry (Johannesbg). 2011;14:316, 318.
5 ACTH-Secreting NETs, AACE Clinical Case Rep. 2015;1(No. 4) e Steinberg P. Adrenal carcinoma and hypertension presenting with catatonic stupor. Aust N Z J Psychiatry. 1996;30: Torpy DJ, Mullen N, Ilias I, Nieman LK. Association of hypertension and hypokalemia with Cushing s syndrome caused by ectopic ACTH secretion: a series of 58 cases. Ann N Y Acad Sci. 2002;970: Hoefer PF, Glaser GH. Effects of pituitary adrenocorticotropic hormone (ACTH) therapy; electroencephalographic and neuropsychiatric changes in fifteen patients. J Am Med Assoc. 1950;143: Acute adverse reactions to prednisone in relation to dosage. Clin Pharmacol Ther. 1972;13: Kelly WF. Psychiatric aspects of Cushing s syndrome. QJM. 1996;89: Haskett RF. Diagnostic categorization of psychiatric disturbance in Cushing s syndrome. Am J Psychiatry. 1985;142: Northoff G, Kötter R, Baumgart F, et al. Orbitofrontal cortical dysfunction in akinetic catatonia: a functional magnetic resonance imaging study during negative emotional stimulation. Schizophr Bull. 2004;30: Scheuerecker J, Ufer S, Käpernick M, et al. Cerebral network deficits in post-acute catatonic schizophrenic patients measured by fmri. J Psychiatr Res. 2009;43: Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 2009;10: Ryan SA, Costello DJ, Cassidy EM, Brown G, Harrington HJ, Markx S. Anti-NMDA receptor encephalitis: a cause of acute psychosis and catatonia. J Psychiatr Pract. 2013;19:
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