The Journal of Clinical Endocrinology & Metabolism Vol. 89, No. 12 6005-6009
Copyright © 2004 by The Endocrine Society
Identification of Patients with Cushing’s Disease with Negative Pituitary Adrenocorticotropin Gradients during Inferior Petrosal Sinus Sampling: Prolactin as an Index of Pituitary Venous Effluent
James W. Findling,
Michael E. Kehoe and
Hershel Raff
Endocrine-Diabetes Center (J.W.F.), Endocrine Research Laboratory (H.R.), and Department of Radiology (M.E.K.), St. Luke’s Medical Center, Milwaukee, Wisconsin 53215; and Department of Medicine (J.W.F., H.R.), Medical College of Wisconsin, Milwaukee, Wisconsin 53226
Address all correspondence and requests for reprints to: Hershel Raff, Ph.D., Endocrinology, St. Luke’s Physician’s Office Building, 2801 West Kinnickinnic River Parkway, Suite 245, Milwaukee, Wisconsin 53215. E-mail: hraff{at}mcw.edu.
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Abstract
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Inferior petrosal sinus sampling for ACTH differentiates pituitary ACTH-dependent Cushing’s (CD) from the ectopic ACTH syndrome (EAS). Petrosal sinus to peripheral (IPS:P) ACTH ratios greater than 2.0 in the basal state or a peak greater than 3.0 after CRH are diagnostic of CD. However, false-negative rates of 1–10% have been reported. We report three patients with features of CD with peak IPS:P ACTH ratios less than 3.0 after CRH suggesting EAS. We compared IPS:P prolactin (PRL) as an index of pituitary venous effluent in these three index cases with 44 patients with CD and five with EAS. The dominant basal IPS:P PRL ratio was greater than 1.8 in all 49 patients but was less than 1.2 in the three index cases. The IPS:P ACTH ratio normalized to IPS:P PRL was greater than 0.8 in all CD patients but was less than 0.6 in EAS patients. The IPS:P ACTH ratios normalized to IPS:P PRL were greater than 1.2 in the index cases, which was similar to those with CD. The three index cases had clinical and biochemical remissions after pituitary surgery.
PRL is an index of pituitary venous effluent during inferior petrosal sinus sampling in patients with CD who fail to have a peak IPS:P ACTH ratio greater than 3.0 after CRH. IPS:P PRL should be measured when results indicate EAS.
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Introduction
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INFERIOR PETROSAL SINUS sampling (IPSS) for ACTH is the best means to distinguish pituitary ACTH-dependent Cushing’s syndrome (Cushing’s disease) from the ectopic ACTH syndrome (1, 2, 3, 4). Although early studies with IPSS-ACTH reported a diagnostic sensitivity and specificity approaching 100% (5, 6), additional experience has revealed some false-negative results. Using a petrosal sinus to peripheral ACTH ratio greater than 2.0 in the basal state or a peak ratio greater than 3.0 after CRH administration, a false-negative rate of 1–10% in patients with proven Cushing’s disease has been reported (7, 8, 9, 10). Although the majority of patients with noncentralizing inferior petrosal sinus to peripheral ratios have nonpituitary ACTH-secreting neoplasms, there has been a failure to localize ectopic ACTH-secreting tumors in a few patients (5, 6).
False-negative results with IPSS have been attributed to either technical problems due to unsuccessful IPSS catheterization or anomalous venous drainage (9). We report three patients with surgically proven pituitary ACTH-dependent Cushing’s syndrome whose peak petrosal sinus to peripheral ACTH ratio was less than 3.0 after CRH. This resulted in the misclassification of these patients as having an occult ectopic ACTH-secreting tumor. Previous studies have suggested that the measurement of other anterior pituitary hormones might be useful during IPSS (11, 12, 13, 14, 15, 16, 17, 18, 19). We now report the retrospective diagnosis of Cushing’s disease with the measurement of prolactin (PRL) from the inferior petrosal sinus (IPSS-PRL) as an index of pituitary venous effluent.
Comparing the results of IPSS-PRL in these three patients with those in archived samples from 44 patients with surgically proven Cushing’s disease and five subjects with ectopic ACTH-secreting neoplasms, we confirmed that pituitary venous effluent had not been properly obtained. Using IPSS-PRL as an index of pituitary venous drainage, we confirmed the presence of a pituitary source of ACTH hypersecretion and offered all three patients corrective pituitary microsurgery.
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Patients and Methods
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Index cases
Table 1
shows the clinical features of the index cases. All three patients had unequivocal ACTH-dependent hypercortisolism as demonstrated by elevated plasma ACTH, late-night salivary cortisol, and elevated urine free cortisol. Whereas cases 1 and 3 had completely negative pituitary magnetic resonance imaging, case 2 was equivocal. In case 1, abnormal pituitary tissue was discovered by a very experienced pituitary neurosurgeon; however, histopathology showed no abnormal tissue. It is not unusual to fail to find abnormal tissue during pathological examination of pituitary aspirates. Secondary adrenal insufficiency was defined as a morning cortisol less than 2 µg/dl at 36–72 h after surgery. Although case 1 did not have subnormal cortisol levels after surgery, she had a clinical and biochemical remission as demonstrated by normal late-night salivary cortisol and 24-h urine free cortisol 6 wk after surgery as well as a dramatic resolution of the clinical features of hypercortisolism. In case 2, the 3-mm focal corticotroph hyperplasia was confirmed by an experienced pituitary histopathologist.
Like others, we have encountered variations in venous anatomy during IPSS including filling of the vertebral venous plexuses as described previously (20). The inferior petrosal sinus catheter position was acceptable when contrast injection filled the ipsilateral inferior petrosal and cavernous sinuses and cross-filled to the contralateral cavernous and inferior petrosal sinuses (Fig. 1). All of the index cases demonstrated filling of the branches of the vertebral venous plexuses, which is not unusual (20).
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FIG. 1. Digital subtraction angiographic radiographs from IPS sampling in the three index cases. Notice the retrograde flux of contrast to the contralateral cavernous sinus.
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Table 2 indicates a post-CRH ACTH inferior petrosal sinus (IPS) to peripheral (IPS:P) ratio of less than 3 in all three index cases. A search for an ectopic neoplasm was negative in cases 1 and 3, whereas an islet cell tumor was discovered in case 2, which, upon resection, was found to be positive for CRH immunostaining but negative for ACTH. All three index cases had plasma CRH levels below the reference interval. Hypercortisolism persisted in case 2 after pancreatic surgery.
The IPSS method has been described previously (5). Informed consent was obtained for all procedures. All 49 patients had successful catheterization of both IPSs. Archived IPSSs from the three index cases, and from patients with surgically proven Cushing’s disease (n = 44; age 12–74 yr, eight males, 36 females) and ectopic ACTH syndrome [n = 5 (three bronchial carcinoids, two neuroendocrine carcinomas); age 48–79 yr, two males, three females] were studied. These samples were stored at –20 C for no more than 3 yr. Basal IPS and peripheral samples were analyzed for each patient. Sets of IPS and peripheral samples at 2, 5, or 10 min after CRH administration (100 µg) were selected based on their peak ACTH response. PRL levels in basal and post-CRH samples were assayed by immunoradiometric assay (Diagnostic Products, Los Angeles, CA).
First, the dominant (peak) post-CRH IPS to peripheral ACTH ratios are presented (and have no units), which is the standard criterion for the differential diagnosis of ACTH-dependent Cushing’s syndrome. The dominant IPS was defined as the highest ACTH IPS:P ratio at 2, 5, or 10 min after CRH injection. Then basal (pre-CRH) ipsilateral IPS to peripheral PRL ratios are presented. Finally, the post-CRH dominant petrosal sinus to peripheral ACTH ratio was divided by the basal ipsilateral IPS to peripheral PRL concentration (see formula below). These PRL-normalized peak ACTH IPS to peripheral ratios also have no units.
There are alternate methods of normalizing IPS ACTH to PRL ACTH (19). Our method was chosen because we were not using this approach to improve lateralization of ACTH secretion, it requires minimal assumptions about the distribution of PRL effluent from normal pituitary tissue, and it parallels the validated method for normalizing aldosterone to cortisol levels during adrenal vein sampling when evaluating hyperaldosteronism (21).
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Results
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All patients with proven Cushing’s disease (pituitary) had peak, post-CRH dominant IPS:P ratios greater than 4.8 (Fig. 2, left panel). All proven ectopic ACTH patients had peak, post-CRH dominant IPS:P ratio less than 2.2. The IPS to peripheral ACTH ratios for the three index cases ranged from 1.2 to 2.7, which was consistent with ectopic ACTH (Table 2
and Fig. 2). Note that the three index cases had a brisk peripheral ACTH response to CRH (Table 2).
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FIG. 2. IPS:P ratios for patients with proven Cushing’s disease (pituitary; circles), ectopic ACTH syndrome (ectopic; squares), and the three index cases (triangles). The left panel is the post-CRH IPS to peripheral ACTH ratio. The middle panel is the basal (pre-CRH) IPS to peripheral PRL ratio from the same sites as the ACTH ratios. The right panel is the left panel divided by the middle panel giving IPS:P ratios normalized to the ipsilateral PRL ratio. Notice the overlap of the IPS-peripheral ACTH ratio for the ectopic ACTH and index cases, that the index cases had IPS-peripheral PRL ratios that were lower than in pituitary and ectopic ACTH, and that normalizing the peak ACTH IPS:P ratio to the ipsilateral PRL ratio led to results in index cases (with subsequently proven Cushing’s disease) similar to prospectively proven pituitary Cushing’s disease.
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All of the patients with proven Cushing’s disease and ectopic ACTH had basal PRL IPS:P ratios greater than 1.8 (Fig. 1, middle panel), indicating successful IPS catheterization. In contrast, the index cases had basal PRL IPS:P ratios less than 1.2, making the fidelity of the catheterization suspect. Of the 44 patients with Cushing’s disease, 21 exhibited a greater than 10% increase in PRL in the dominant petrosal sinus in response to CRH. None of the five patients with ectopic ACTH showed an increase in petrosal sinus PRL levels in response to CRH (P < 0.061 by Fisher’s exact test).
To account for possible anomalous venous drainage, the peak dominant IPS:P ACTH ratios were each normalized to the basal IPS:P PRL ratios in the samples from the corresponding anatomic sites (Table 2 and Fig. 2, right panel). The PRL-normalized ACTH IPS:P ratios were all greater than 0.8 in patients with proven Cushing’s disease, whereas they were all less than 0.6 in patients with proven ectopic ACTH syndrome. The PRL-normalized ACTH IPS:P ratios were 1.3–2.4 in the index cases, making them consistent with pituitary Cushing’s disease.
As shown in Table 1, all three index case underwent pituitary surgery in which abnormal pituitary tissue was identified and a clinical remission or frank secondary adrenal insufficiency ensued postoperatively.
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Discussion
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This report describes three patients with surgically proven Cushing’s disease in whom inferior petrosal sinus sampling failed to demonstrate a pituitary ACTH gradient despite technically successful procedures. Using PRL as an index of pituitary venous effluent, we recognized that pituitary venous blood had not been accurately sampled. We then normalized the peak post-CRH IPS:P ACTH ratios to basal PRL from the same site. Comparing these results with archived IPSSs from patients with surgically proven Cushing’s disease and ectopic ACTH syndrome, we identified a pituitary source of ACTH hypersecretion in these three patients and recommended corrective pituitary microsurgery.
Although IPSS is the best diagnostic study to differentiate Cushing’s disease from the ectopic ACTH syndrome, anomalous venous drainage may result in diagnostic errors during the procedure, and false-negative rates of 1–10% have been reported (7, 8, 9, 10). A petrosal sinus to peripheral ACTH ratio greater than 2.0 in the basal state or peak ratio greater than 3.0 after CRH administration is considered diagnostic of Cushing’s disease (6). Recently, however, Swearingen et al. (10) reported a diagnostic sensitivity of IPSS of 85% with a basal IPS:P ratio greater than 2 and 90% with a post-CRH IPS:P ratio greater than 3.0.
The failure to demonstrate a significant pituitary ACTH gradient with IPSS in patients with Cushing’s disease may have several possible explanations. Anatomical variations in the veins draining the IPSs may cause technical difficulty during catheterization (9, 20, 22, 23). Correct catheter placement is considered satisfactory if both IPSs are cannulated as demonstrated by retrograde flow of contrast into the contralateral cavernous sinus both before and after sampling (22). Despite achieving good catheter localization in our three patients (Fig. 1), we obtained false-negative results and misclassified these patients with the occult ectopic ACTH syndrome. Dilution of petrosal venous blood by a nonpituitary source, depending on how aggressively the catheters are advanced into the petrosal sinus, may also account for differences in sensitivity. For example, jugular vein sampling for ACTH has been proposed as an alternative to IPSS (24, 26); however, venous admixture in the jugular bulb may be quite significant, yielding a diagnostic sensitivity of only 75–80% (24). Obviously, an unusual location of a corticotroph adenoma (i.e. the sphenoid sinus) may not drain into the cavernous sinus and the IPS. Finally, it seems quite likely that anomalous venous drainage of the anterior pituitary hormone may account for the failure of technically successful IPSS to yield a pituitary ACTH gradient in patients with Cushing’s disease (27).
To verify the fidelity of pituitary venous drainage, we retrospectively measured PRL levels in three patients without a pituitary ACTH gradient in whom imaging studies failed to demonstrate an ectopic ACTH-secreting neoplasm. These results were compared with those from archived IPSSs in 44 patients with proven Cushing’s disease and five with a proven ectopic ACTH-secreting tumor. The central PRL to peripheral ratio was less than 1.1 in these three patients but was greater than 1.8 in all the patients with surgically proven ACTH-dependent Cushing’s syndrome. We then adjusted the dominant peak petrosal sinus to peripheral ACTH gradient by normalization to the basal ipsilateral petrosal sinus to peripheral PRL ratio to account for abnormal pituitary venous drainage. Petrosal sinus to peripheral ACTH ratio normalized to PRL was greater than 0.8 in all patients with Cushing’s disease but was less than 0.6 in all patients with the ectopic ACTH syndrome. The dominant peak petrosal sinus to peripheral ACTH ratio normalized to PRL was greater than 1.3 in our three patients. Interestingly, one of our patients actually had a neuroendocrine (islet cell) tumor of the pancreas discovered, which had positive immunocytochemistry for CRH but negative staining for ACTH. Endogenous hypercortisolism persisted after the removal of this tumor. Case 3 was a man with prodigious hypercortisolism and profound hypokalemia whose clinical picture certainly suggested the ectopic ACTH syndrome. He was treated medically with ketoconazole and metyrapone for 2 yr before we reanalyzed his IPSS and correctly characterized him as having pituitary ACTH-dependent hypercortisolism. In retrospect, all three index cases also had brisk peripheral ACTH responses to CRH, a finding more commonly seen in patients with Cushing’s disease than ectopic ACTH (10, 28). Finally, all three of these patients had clinical and biochemical remissions of their Cushing’s disease after pituitary surgery.
This study confirms and extends the value of measuring PRL as a surrogate of pituitary venous drainage. McNally et al. (19) reported the use of PRL and TSH after TRH administration as a reliable method for correcting the dilution from nonpituitary venous blood during IPSS. They reported eight patients with Cushing’s disease in whom the central to peripheral ACTH ratio was misdiagnosed in four. After they corrected the ACTH ratios for TRH-stimulated PRL and TSH, all the patients were correctly identified with pituitary-dependent Cushing’s syndrome. Unfortunately, TRH is no longer available for diagnostic use in the United States. Furthermore, McNally et al. made the decision to normalize based on the intersinus ratio of PRL, which required the assumption that intersinus PRL ratio should be close or equal to unity. Our approach of normalizing the dominant post-CRH ACTH IPS:P ratio to the ipsilateral basal PRL IPS:P ratio involved no such assumptions and was not confounded by CRH stimulation of PRL (11, 12). Finally, the main objective of McNally et al. (19) was to improve lateralization of the pituitary tumor, which was also the main objective of several other studies measuring multiple pituitary hormones during IPSS (14, 15). An earlier study (16) also attempted to use PRL and TSH to lateralize ACTH secretion during IPSS; at that time, CRH was not available for use during IPSS, so it is difficult to assess the usefulness of their approach in the differential diagnosis of ACTH-dependent Cushing’s syndrome.
Many of our patients (48%) with Cushing’s disease had increases in PRL after CRH administration. Therefore, we used the basal PRL concentration from the inferior petrosal sinus and the peripheral sample to correct for possible abnormal venous drainage. Other investigators reported similar increases in PRL after CRH in some patients with Cushing’s disease. Loli et al. (12) reported that 11 of 22 patients with Cushing’s disease had CRH-induced PRL increases during IPS, but none of the pituitary tumors showed positive immunocytochemistry for PRL. Actually, CRH also stimulated GH in 13 of 20 of these patients, yet none of the tumors demonstrated positive immunocytochemistry for GH. Schulte and Monig (11) also showed that CRH provoked PRL and ACTH in the petrosal sinus on the same side the corticotroph adenoma was found, but there was no PRL increase in one patient with the ectopic ACTH syndrome.
Because glucocorticoids inhibit PRL release (29), we were concerned that endogenous hypercortisolism might attenuate PRL secretion and abolish the presence of a pituitary PRL gradient. However, all the patients with successful IPSS had IPSS:P to PRL ratios of 1.8 or greater, and our three index cases had IPS:P to PRL ratio less than 1.2. In other words, the measurement of PRL from petrosal sinus and peripheral venous blood should confirm the fidelity of the sampling procedure. Moreover, it appears that normalization of the CRH stimulated peak dominant IPS:P-ACTH to the basal IPS:P-PRL will correctly classify the patient with Cushing’s disease in whom there was not a significant petrosal sinus ACTH gradient and therefore help to eliminate false-negative results. We have not yet encountered a patient with a proven ectopic ACTH-secreting neoplasm in whom IPSS failed to obtain satisfactory pituitary venous effluent. Of course, such a patient would be suspected to have an IPS:P to PRL ratio less than 1.1, but the normalized ACTH to PRL ratio might look similar to patients with Cushing’s disease.
In summary, the measurement of PRL (as an index of fidelity of pituitary venous effluent during IPSS) and the establishment of a normalized ACTH/PRL petrosal sinus to peripheral ratio will identify patients with Cushing’s disease who fail to have a peak IPS:P to ACTH ratio greater than 3.0 after CRH. This may be particularly important if the patients shows a robust peripheral ACTH response to CRH. We strongly recommend that any patient with a petrosal sinus to peripheral ACTH ratio of less than 3.0 after CRH should have inferior petrosal sinus and peripheral samples analyzed for PRL to ensure adequate venous sampling.
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Acknowledgments
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The authors thank Eric Bruder, Barbara Jankowski, Peter Homar, and the staff of the Interventional Radiology Department at St. Luke’s Medical Center.
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Footnotes
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Abbreviations: IPS, Inferior petrosal sinus; IPS:P, IPS to peripheral ratio; IPSS, inferior petrosal sinus sampling; PRL, prolactin.
Received July 15, 2004.
Accepted September 21, 2004.
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Abstract
Introduction
