False-positive inferior petrosal sinus sampling in the diagnosis of Cushing s disease
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1 J Neurosurg 83: , 1995 False-positive inferior petrosal sinus sampling in the diagnosis of Cushing s disease Report of two cases YOSHIHIRO YAMAMOTO, M.D., D.M.SC., DUDLEY H. DAVIS, M.D., TODD B. NIPPOLDT, M.D., WILLIAM F. YOUNG, JR., M.D., JOHN HUSTON III, M.D., AND JOSEPH E. PARISI, M.D. Departments of Neurosurgery, Internal Medicine, Neuroradiology, and Neuropathology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota Inferior petrosal sinus sampling (IPSS) for adrenocorticotropic hormone (ACTH) levels in patients with Cushing s syndrome has become a useful method to distinguish ACTH-secreting pituitary tumors (Cushing s disease) from other causes of the syndrome, principally ectopic adrenocorticotropin secretion by an occult tumor. Although the test is generally regarded as highly specific, the authors recently encountered two patients whose IPSS measurements were falsepositive for Cushing s disease. The results of IPSS suggested a pituitary origin of ACTH secretion in both patients, but transsphenoidal surgery failed to disclose a pituitary adenoma or to improve postoperative plasma cortisol levels. Both patients subsequently were found to have an ACTH-secreting carcinoid tumor of the lung. The false-positive IPSS studies were due to periodic hormonogenesis. The patients must be hypercortisolemic at the time IPSS is performed for the study to be valid. KEY WORDS Cushing s syndrome Cushing s disease inferior petrosal sinus sampling carcinoid tumor T HE diagnosis and differential diagnosis of Cushing s syndrome had been one of the most perplexing problems in endocrinology until relatively recently, when bilateral inferior petrosal sinus sampling (IPSS) of plasma became available. In 1977, Corrigan, et al., 2 reported one of the first cases in which a pituitary origin of adrenocorticotropic hormone (ACTH) production was identified through IPSS. In their analysis of 246 patients with Cushing s syndrome, Oldfield and colleagues 16 used IPSS with and without ovine corticotropin releasing hormone (ocrh) and found no false-positive results (specificity 100%) in identifying Cushing s disease in basal samples when the inferior petrosal sinus (IPS)/plasma (P) ratio was equal to or greater than 2. They reported that a peak IPS/P ACTH ratio equal to or greater than 3 after ocrh administration identified all patients with Cushing s disease (sensitivity 100%) with no false-positive results (specificity 100%). In patients with Cushing s disease, the ACTH gradient in the two sinuses predicted the location of a microadenoma in approximately 70% of patients. We have used IPSS with ocrh stimulation since 1990 in 70 patients and have found it to be reliable. Recently, however, we encountered two patients with Cushing s syndrome whose results on IPSS for ACTH suggested a pituitary origin of ACTH secretion. Neither patient improved after transsphenoidal surgery, and no pituitary adenoma was found in the surgical specimen. Both patients subsequently were found to have ACTH-secreting bronchial carcinoid tumors. Case Reports Case 1 This 33-year-old woman developed skin pigmentation and significant weight gain during the year prior to presentation to her local physician. Laboratory studies revealed a morning cortisol level of 18.7 g/dl, an ACTH level of 89 pg/ml (normal 0 60), and a 24-hour urine free cortisol (UFC) of 221 g (normal ). Both overnight low-dose (1 mg) and high-dose (8 mg) dexamethasone suppression tests (DSTs) were nonsuppressive (plasma cortisol 13 g/dl with both tests). A computerized tomography (CT) scan of the head showed a possible microadenoma on the left side of the pituitary gland. Results 1087
2 Y. Yamamoto, et al. TABLE 1 Results of inferior petrosal sinus sampling in Case 1* ACTH (pg/ml) Time (min) RPS LPS P * Abbreviations: ACTH = adrenocorticotropic hormone; LPS = left petrosal sinus; P = peripheral blood plasma sample; RPS = right petrosal sinus; = not done. Time before and after administration of ovine corticotropin releasing hormone (1 g/kg). of IPSS performed at the patient s local medical center showed a right IPS/P ratio of 168/39 = 4.31, and left IPS/P of 47/39 = 1.21 with ocrh stimulation, suggesting that the ACTH secretion originated from the right side of the pituitary gland (Table 1). Cortisol levels were not examined on the day of IPSS. The diagnosis of Cushing s syndrome was questioned because two subsequent UFC measurements 7 and 8 days after the IPSS study were 39 and 41 g per 24 hours, respectively (normal 50 g/24 hours). The patient came to the Mayo Clinic for further evaluation. The repeated morning cortisol level was 31 g/dl (normal 25) with an evening cortisol level of 19 g/dl (normal 14). The 24-hour UFC was 200 g/24 hours (normal ). Both ketogenic steroids and 17-ketosteroids were increased at 15 mg/24 hours (normal 2 12) and 18 mg/24 hours (normal 4 17), respectively. Dexamethasone suppression testing showed a 24-hour UFC FIG. 1. Case 1. Coronal view of a computerized tomography scan showing the head after contrast injection. There is a 3- to 4- mm nonenhancing area in the sella turcica on the left side of the midline, indicating a possible microadenoma. FIG. 2 Case 1. A computerized tomography scan of the chest showing a 1-cm indeterminate nodule in the right midlung. level of 61 g/24 hours with low-dose DST, and 50 g/24 hours with high-dose DST. Repeat CT scan of the head revealed the sella and pituitary gland to be of normal size. There was a 3- to 4-mm diameter area of low attenuation on the left side of the midline after injection of contrast medium (Fig. 1). A magnetic resonance (MR) image was not obtained because of the patient s claustrophobia. A CT scan of the chest showed a 1-cm indeterminate nodule in the right midlung (Fig. 2). The patient underwent a complete right hemihypophysectomy and subtotal left hemihypophysectomy, but no adenoma was found on biopsy. Postoperatively, the patient s 24-hour UFC level remained high, at 225 g/24 hours. A right thoracotomy and right middle lobectomy were performed 2 months after the transsphenoidal surgery, and a 1-cm carcinoid tumor was found in the surgical specimen. Histologically, the tumor demonstrated the classic appearance of a carcinoid composed of solid nests of relatively uniform small cells with regular nuclei. Immunohistochemical staining showed strong immunoreactivity to chromogranin but none to ACTH. In situ hybridization staining for ACTH was positive. The patient s cortisol level diminished to less than 1 g/dl postoperatively. Case 2 This 38-year-old woman with a 2-year history of hypertension noted facial swelling, significant weight gain, acne, and hirsutism. She had no visual symptoms. Evaluation at another institution showed a markedly elevated 24-hour UFC of 2265 g (normal ) and plasma ACTH levels of 35 and 159 pg/ml (normal 0 60). The 8- mg overnight DST showed suppression consistent with pituitary disease (plasma cortisol 17 g/dl at baseline and suppressed to 4.2 g/dl). Evaluation at the Mayo Clinic revealed a morning cortisol level of 20 g/dl and a 24- hour UFC level of 96 g (normal ). Inferior petrosal sinus sampling showed no baseline IPS/P gradient, but a significant gradient (12:1) was found with ocrh in the left IPS (Table 2). Both CT scans and MR images failed to show evidence of a pituitary lesion. A chest CT showed a 1-cm nodule in the right midlung posteriorly, but ra- 1088
3 False-positive petrosal sampling for Cushing s disease TABLE 2 Results of inferior petrosal sinus sampling in Case 2* ACTH (pg/ml) Cortisols ( g/dl) Time (min) RPS LPS P P * Abbreviations: ACTH = adrenocorticotropic hormone; LPS = left petrosal sinus; P = peripheral blood plasma sample; RPS = right petrosal sinus; = not done. Time before and after administration of ovine corticotropin releasing hormone (1 g/kg). TABLE 3 Etiology of Cushing s syndrome* ACTH dependent pituitary corticotropic adenoma corticotropic multinodular hyperplasia ectopic ACTH-secreting tumor CRH-secreting tumor ACTH- and CRH-secreting tumor ACTH independent unilateral adrenal disease adenoma carcinoma bilateral adrenal disease macronodular hyperplasia primary pigmented nodular adrenal disease * Abbreviations: ACTH = adrenocorticotropic hormone; CRH = corticotropin releasing hormone. diographically this lesion was indeterminate. Transsphenoidal surgery did not reveal pituitary adenoma, and a near-total anterior hypophysectomy was performed. After surgery, the morning plasma cortisol level was 5.5 g/dl. Two months later, however, the morning plasma cortisol was 56 g/dl and the 24-hour UFC was The patient s postoperative course was complicated by a compression fracture of L-4 and T-12 from severe osteoporosis. The patient subsequently developed necrotizing Aspergillus bronchopneumonia and died 3 months after surgery. The postmortem study revealed a 1-cm bronchial carcinoid tumor in the posterior segment of the right upper lung. The classic features of a carcinoid were demonstrated by histological analysis. Immunohistochemical staining showed strong immunoreactivity to chromogranin and ACTH. Discussion The etiology of Cushing s syndrome can be divided into two principal categories: ACTH dependent, which comprises approximately 80% of cases, and ACTH independent, which comprises approximately 20%. 19 The former includes ACTH-secreting pituitary adenomas (Cushing s disease), ectopic ACTH-secreting tumors, and ectopic tumors that secrete corticotropin-releasing hormone (CRH) or related peptides (Table 3). The prevalence of the pituitary origin is reported to be approximately 80% of the ACTH-dependent group, whereas the ectopic origin represents approximately 15%. The ACTH-independent group includes adrenal adenoma (approximately 80%), adrenal carcinoma (approximately 20%), macronodular hyperplasia, and primary pigmented nodular adrenal disease (less than 1% each). Recent advances in assay techniques and their wide availability make it possible to diagnose Cushing s syndrome earlier in the natural history of the illness, possibly when the clinical signs are subtle and disabilities less severe. A potential problem in diagnosing ACTH-dependent Cushing s syndrome is the cyclic or intermittent activity of the disease seen in some patients. 1 In patients with Cushing s syndrome, the normal diurnal rhythm of cortisol secretion is usually lost. Nonendocrine illnesses such as heart failure, infection, depression, and alcoholism can also alter this normal diurnal rhythm, making plasma cortisol unreliable as a primary marker. Furthermore, pregnancy, oral contraceptive use, and estrogen-secreting tumors can induce the production of cortisol-binding globulin in the liver, raising the measured total plasma cortisol level. The biochemical diagnosis of Cushing s syndrome relies upon demonstrating excess integrated cortisol secretion and abnormal feedback regulation of the hypothalamo-pituitary-adrenal axis. The former is usually determined by measuring urinary glucocorticoids, the latter with dynamic stimulation and suppression tests. The diagnostic evaluation of Cushing s syndrome at our institution typically proceeds as outlined in Table 4. First, hypercortisolism must be suspected based on the known manifestations of the disorder, then confirmed with measurements of serum and 24-hour UFC concentrations. A recent survey of 146 patients with Cushing s syndrome confirmed a sensitivity of 95% but also noted that, in 11% of patients, at least one of four UFC measurements was TABLE 4 Process of diagnostic evaluation of Cushing s syndrome at Mayo Clinic* confirmation of hypercortisolism clinical assessment baseline glucocorticoids (serum cortisol levels, UFC excretion) and low-dose DST subtype diagnosis plasma ACTH high-dose DST IPPS for ACTH with ocrh stimulation localization studies directed computerized imaging IPSS for ACTH with ocrh stimulation * Abbreviations: ACTH = adrenocorticotropic hormone; DST = dexamethasone suppression test; IPSS = inferior petrosal sinus sampling; ocrh = ovine corticotropin releasing hormone; UFC = urinary-free cortisol. 1089
4 Y. Yamamoto, et al. within the normal range. If three or four UFC collections are normal, the diagnosis of Cushing s syndrome is extremely unlikely. 19 Classic assays for urinary 17-oxogenic steroids (17-OGS) and 17-hydroxycorticosteroids (17- OHCS) have higher false-negative and false-positive rates. Thus, the measurement of 17-OGS or 17-OHCS has been excluded from screening tests for Cushing s syndrome. 19 Dexamethasone, which does not cross-react in most cortisol radioimmunoassays, has been used in the diagnosis and differential diagnosis of Cushing s syndrome for 35 years. Autonomous hypercortisolism (Cushing s syndrome) is confirmed by the low-dose DST (0.5 mg dexamethasone administered orally every 6 hours for 48 hours); a 24-hour UFC excretion greater than or equal to 20 g with low-dose dexamethasone administration establishes the diagnosis. The low-dose DST is not necessary in patients with obvious stigmata on physical examination and baseline 24-hour UFC measurements greater than threefold above the upper limit of normal. Phenytoin, rifampicin, phenobarbital, and other drugs that induce liver enzymes increase the clearance rate of dexamethasone and can result in a false-negative suppression. Once the diagnosis of Cushing s syndrome has been established, investigations should be directed at identifying the precise cause of the disease. The classic ectopic ACTH syndrome can be distinguished clinically from Cushing s disease by a short duration of illness, weight loss, severe myopathy, pigmentation, and hypokalemia. This syndrome is also associated with overt neoplasms and markedly high plasma ACTH levels. Small occult ectopic ACTH-secreting tumors, however, may present with a clinical picture identical to that seen in patients with Cushing s disease. These tumors can be difficult to distinguish biochemically. Plasma ACTH concentration is of limited value in distinguishing between the causes, because there is a large overlap, although markedly high levels favor ectopic production. Detection of big- ACTH, which is produced by abnormal processing of an ACTH precursor, usually indicates ectopic secretion, although on rare occasions it can be pituitary in origin. 6 In patients with ACTH-dependent hypercortisolism, the high-dose DST (2 mg dexamethasone administered orally every 6 hours for 48 hours) helps differentiate pituitary from ectopic ACTH hypersecretion; a 24-hour UFC excretion that decreases 50% or more from baseline values is consistent with pituitary-dependent disease. The overall accuracy with more than 50% suppression is 80%; if more than 90% suppression is found, the accuracy of this test increases to 86%. 5 The overnight 8-mg DST may be substituted for the 2-day high-dose study. Dexamethasone is administered at 11:00 p.m. in a single 8-mg dose. Plasma for cortisol measurement is drawn the next morning at 8:00 a.m. The criterion for positive response (suppressibility) is a plasma cortisol level 50% or less than the baseline level, a finding consistent with pituitary disease (sensitivity 89%, specificity 100%). 10 However, some types of ectopic ACTH-secreting tumors (for example, bronchial carcinoid) may also suppress cortisol with high-dose dexamethasone administration. 11 The ocrh test induces a rise in circulating ACTH and cortisol in normal subjects, whereas in patients with Cushing s disease this response tends to be exaggerated. Patients with the ectopic ACTH syndrome typically have no response to ocrh. 7 A recent analysis of Cushing s disease showed a true-positive rate of approximately 90%. The medical literature shows scattered case reports of patients with ectopic ACTH secretion responding to ocrh with a rise in cortisol. 12 Approximately 70% of patients with the ectopic ACTH syndrome cosecrete at least one additional peptide, such as carcinoembryonic antigen, somatostatin, gastrin, calcitonin, bombesin, pancreatic polypeptide, vasoactive intestinal peptide, glucagon, human chorionic gonadotropin-, CRH, and others. The demonstration of additional ectopic peptide secretion helps differentiate ACTHdependent Cushing s syndrome. 19 Simultaneous bilateral IPSS for ACTH has been developed in the past decade as a means to confirm pituitary ACTH secretion and to lateralize the tumor within the pituitary fossa. 2,4,11,13,15,16 Although concerns have arisen about the feasibility of catheterizing both IPSs consistently and safely, Oldfield and associates 16 successfully performed the procedure in 281 of 284 consecutive patients without major complications. Major neurological complications have occurred in only 0.2% of procedures (one of 508) performed at the National Institutes of Health. 14 In the one case with major complications, the patient developed brainstem injury related to difficult catheterization and subsequent venous hypertension. Oldfield, et al., 16 reported that patients with Cushing s disease were distinguished from patients with ectopic ACTH secretion by basal IPSS, with a diagnostic accuracy of 96% applying to IPS/P ratios of equal to or greater than 2. After ocrh stimulation, IPSS with an IPS/P ratio cut-off at 3 or greater had a diagnostic accuracy of 100% in the 246 patients with an established diagnosis. In earlier studies, various IPSS/P ratio cut-offs were reported ranging from 1.4 to 2, but in a much smaller number of cases. 4,15,20 The assessment of the value of IPSS in the lateralization of tumors in the pituitary gland is difficult, because tumors may be midline or have anomalous venous drainage. 8 To lateralize the pituitary adenoma, Oldfield and associates 15 first used a gradient of greater than 1.4 as significant and reported accurate lateralization in all 10 of their patients. Trainer and colleagues 20 used a gradient of greater than 2 as significant and, with ocrh stimulation, they confirmed localization at surgery in 66% of patients. In a more recent report, using a gradient of 1.4 or greater, Oldfield and associates 16 predicted the location of the adenoma in 68% of patients during basal sampling and in 71% after ocrh stimulation. To date, the literature contains no reports of false-positive IPSS for patients with Cushing s disease in whom ectopic ACTH-secreting carcinoid tumors were histologically proven. Both of our patients had positive IPSS with ocrh, but both had relatively normal cortisol secretion at the time of IPSS. Oldfield and associates 16 stated that correct interpretation of the results of IPSS requires that the patient be in a hypercortisolemic state. Suppression of the pituitary secretion of adrenocorticotropin through sustained hypercortisolism accounts for the absence of a central-to-peripheral adrenocorticotropin gradient in patients with ectopic adrenocorticotropin syndrome and primary adrenal disease. Thus, three situations may produce a 1090
5 False-positive petrosal sampling for Cushing s disease false-positive central-to-peripheral ACTH gradient in the patient with ectopic Cushing s syndrome: 1) therapy to return cortisol production to normal; 2) the presence of intermittent Cushing s syndrome (periodic hormonogenesis); or 3) ectopic CRH secretion. Repeating the IPSS when the patient is hypercortisolemic is a reasonable course of action to confirm positive findings if the concurrent cortisol levels are in the normal range. Radiological imaging of the pituitary gland does not currently play a significant role in the diagnosis of Cushing s disease. Contrast-enhanced CT scans of the sella turcica detected only 30% of the adenomas in one series. 18 Use of MR imaging gave only slightly better results, with a sensitivity rate of 37.5% in the same study. Kaye and Crapo 10 report a sensitivity of 77% for MR images and 47% for CT scans for the detection of pituitary adenomas in Cushing s disease. In a series of 13 patients with suspected Cushing s disease, however, gadolinium-enhanced MR imaging detected 10 of 12 adenomas and revealed no pituitary abnormality in a patient found to have an ectopic source of ACTH. 3 Indeed, approximately 10% of the normal adult population has pituitary abnormalities on MR images that are compatible with pituitary microadenoma. 9 Therefore, even in the presence of a positive image of a pituitary adenoma, this must be interpreted in conjunction with biochemical data. The sustained remission rate of Cushing s disease after transsphenoidal surgery has been reported to be in the range of 74% to 85%. 17,18 In the eight patients who were classified as therapeutic failures in a series by Tindall, et al., 18 three had diagnostic errors, two of which were in patients with a presumed ectopic source of ACTH secretion. Surgery failed in four of the eight patients. Inferior petrosal sinus sampling was not done in either of the patients with a presumed ectopic ACTH tumor. Although Tindall, et al., 18 suggested that the diagnostic errors would have been prevented if they had applied IPSS, we should still keep in mind the possibility of false-positive results with this test. Conclusions In the two patients reported here, the results of IPSS suggested a pituitary origin of ACTH secretion, but transsphenoidal surgery failed to disclose a pituitary adenoma or to improve postoperative plasma cortisol levels. Both patients subsequently were found to have an ACTH-secreting carcinoid tumor of the lung. The false-positive IPSS studies were due to periodic hormonogenesis, and we therefore conclude that the patient must be hypercortisolemic at the time IPSS is performed for the study to be valid. Acknowledgment The authors are grateful to Julie Hipp for editorial assistance. References 1. Atkinson AB, Kennedy AL, Carson DJ, et al: Five cases of cyclical Cushing s syndrome. Br Med J 291: , Corrigan DF, Schaaf M, Whaley RA, et al: Selective venous sampling to differentiate ectopic ACTH secretion from pituitary Cushing s syndrome. N Engl J Med 296: , Fahlbusch R, Buchfelder M: Transsphenoidal surgery of parasellar pituitary adenomas. Acta Neurochir 92:93 99, Findling JW, Aron DC, Tyrrell JB, et al: Selective venous sampling for ACTH in Cushing s syndrome: differentiation between Cushing disease and the ectopic ACTH syndrome. Ann Intern Med 94: , Flack MR, Oldfield EH, Cutler GB Jr, et al: Urine free cortisol in the high-dose dexamethasone suppression test for the differential diagnosis of Cushing syndrome. Ann Intern Med 116: , Fuller PJ, Lim ATW, Barlow JW, et al: A pituitary tumor producing high molecular weight adrenocorticotropin-related peptides: clinical and cell culture studies. J Clin Endocrinol Metab 58: , Gillies G, Grossman A: The CRFs and their control: chemistry, physiology and clinical implications. Clin Endocrinol Metab 14: , Green HT: The venous drainage of the human hypophysis cerebri. Am J Anat 100: , Hall WA, Luciano MG, Doppman JL, et al: Pituitary magnetic resonance imaging in normal human volunteers: occult adenomas in the general population. Ann Intern Med 120: , Kaye TB, Crapo L: The Cushing syndrome: an update on diagnostic tests. Ann Intern Med 112: , Leinung MC, Young WF Jr, Whitaker MD, et al: Diagnosis of corticotropin-producing bronchial carcinoid tumors causing Cushing s syndrome. Mayo Clin Proc 65: , Malchoff CD, Orth DN, Abboud C, et al: Ectopic ACTH syndrome caused by a bronchial carcinoid tumor responsive to dexamethasone, metyrapone, and corticotropin-releasing factor. Am J Med 84: , Manni A, Latshaw RF, Page R, et al: Simultaneous bilateral venous sampling for adrenocorticotropin in pituitary-dependent Cushing s disease: evidence for lateralization of pituitary venous drainage. J Clin Endocrinol Metab 57: , Miller DL, Doppman JL, Peterman SB, et al: Neurologic complications of petrosal sinus sampling. Radiology 185: , Oldfield EH, Chrousos GP, Schulte HM, et al: Preoperative lateralization of ACTH-secreting pituitary microadenomas by bilateral and simultaneous inferior petrosal venous sinus sampling. N Engl J Med 312: , Oldfield EH, Doppman JL, Nieman LK, et al: Petrosal sinus sampling with and without corticotropin-releasing hormone for the differential diagnosis of Cushing s syndrome. N Engl J Med 325: , Ram Z, Nieman LK, Cutler GB Jr, et al: Early repeat surgery for persistent Cushing s disease. J Neurosurg 80:37 45, Tindall GT, Herring CJ, Clark RV, et al: Cushing s disease: results of transsphenoidal microsurgery with emphasis on surgical failures. J Neurosurg 72: , Trainer PJ, Grossman A: The diagnosis and differential diagnosis of Cushing s syndrome. Clin Endocrinol 34: , Trainer PJ, Howlett TA, Dacie JE, et al: Simultaneous bilateral inferior petrosal sinus sampling with 100 mcg corticotrophin releasing hormone (CRH-41) for ACTH in 32 patients with ACTH-dependent Cushing s syndrome. Neuroendocrinology 52 (Suppl 1):145, 1990 (Abstract) Manuscript received January 23, Accepted in final form May 23, Address reprint requests to: Yoshihiro Yamamoto, M.D., D.M.Sc., Department of Neurosurgery, Mayo Clinic, 200 First Street, SW, Rochester, Minnesota
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