Pheochromocytoma. Diagnosis, Localization, and Treatment. National Institute of Child Health and Human Development NIH, Bethesda, USA
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1 Pheochromocytoma Diagnosis, Localization, and Treatment Karel Pacak, MD, PhD, DSc National Institute of Child Health and Human Development NIH, Bethesda, USA Jacques W. M. Lenders, MD, PhD Department of Internal Medicine Division of General Internal Medicine Radboud University Nijmegen Medical Center Nijmegen, The Netherlands Graeme Eisenhofer, PhD National Institute of Neurological Disorders and Stroke NIH, Bethesda, USA
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3 Pheochromocytoma
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5 Pheochromocytoma Diagnosis, Localization, and Treatment Karel Pacak, MD, PhD, DSc National Institute of Child Health and Human Development NIH, Bethesda, USA Jacques W. M. Lenders, MD, PhD Department of Internal Medicine Division of General Internal Medicine Radboud University Nijmegen Medical Center Nijmegen, The Netherlands Graeme Eisenhofer, PhD National Institute of Neurological Disorders and Stroke NIH, Bethesda, USA
6 2007 Karel Pacak, Jacques W. M. Lenders and Graeme Eisenhofer Published by Blackwell Publishing Blackwell Publishing, Inc., 350 Main Street, Malden, MA , USA Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK Blackwell Publishing Asia Pty Ltd, 550 Swanston Street, Carlton, Victoria 3053, Australia The right of the Authors to be identified as the Authors of this Work has been asserted in accordance with the Copyright, Designs and Patents Act All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. First published Library of Congress Cataloging-in-Publication Data Pacak, Karel. Pheochromocytoma : diagnosis, localization, and treatment / Karel Pacak, Jacques W. M. Lenders, Graeme Eisenhofer. p. ; cm. Includes index. ISBN: Pheochromocytoma. I. Lenders, Jacques W. M. II. Eisenhofer, Graeme. III. Title. [DNLM : 1. Pheochromocytoma diagnosis. 2. Diagnosis, differential. 3. Pheochromocytoma genetics. 4. Pheochromocytoma therapy. QZ 380 P113p 2007] RC280.A3P '445 dc A catalogue record for this title is available from the British Library Set in 9/12, Stone serif by Charon Tec Ltd (A Macmillan Company), Chennai, India Printed and bound in Singapore by Fabulous Printers Pte Ltd Commissioning Editor: Alison Brown Editorial Assistant: Jennifer Seward Development Editor: Adam Gilbert Production Controller: Debbie Wyer For further information on Blackwell Publishing, visit our website: The publisher s policy is to use permanent paper from mills that operate a sustainable forestry policy, and which has been manufactured from pulp processed using acid-free and elementary chlorine-free practices. Furthermore, the publisher ensures that the text paper and cover board used have met acceptable environmental accreditation standards. Blackwell Publishing makes no representation, express or implied, that the drug dosages in this book are correct. Readers must therefore always check that any product mentioned in this publication is used in accordance with the prescribing information prepared by the manufacturers. The author and the publishers do not accept responsibility or legal liability for any errors in the text or for the misuse or misapplication of material in this book.
7 Contents 1 Introduction 1 2 Historical comments 3 3 Pathology 4 4 Clinical presentation of pheochromocytoma Signs and Symptoms Differential Diagnosis Special Presentations Diagnosis of Pheochromocytoma in Patients with an Incidentally Discovered Adrenal Mass Pheochromocytoma as an Endocrine Emergency Hypertensive Crisis Hypotension and Shock Multisystem Failure Cardiac Emergencies Acute Peripheral Ischemia Pulmonary Emergencies Gastrointestinal Emergencies Nephrological Emergencies Neurological Emergencies Malignant Pheochromocytoma Pheochromocytoma in Children Pheochromocytoma in Pregnancy Pseudopheochromocytoma Factitious Pheochromocytoma 29 5 Current trends in genetics of pheochromocytoma MEN Syndromes Diagnostic Approaches VHL Syndrome NF Type Succinate Dehydrogenase Gene Related Pheochromocytoma Genetic Problems in Sporadic and Other Pheochromocytomas 38 6 Catecholamines and adrenergic receptors Synthesis and Sources of Catecholamines Synthesis of Catecholamines in Pheochromocytoma Storage and Release of Catecholamines by the Sympathoadrenal System 45
8 vi Contents 6.4 Uptake and Metabolism of Catecholamines Produced by the Sympathoadrenal System Catecholamine Metabolism in Hepatomesenteric Organs Catecholamines Metabolism and Release by Pheochromocytoma Kinetics and Elimination of Catecholamines and Their Metabolites Pharmacology of Catecholamine Systems: Implications for Pheochromocytoma Physiology of Catecholamine Systems Adrenal Medullary Hormone System Peripheral Dopamine Systems Adrenergic Receptors and Their Functions Actions of the Catecholamines 69 7 Current trends in biochemical diagnosis of pheochromocytoma Biochemical Tests of Catecholamine Excess Measurement Methods Reference Intervals Initial Biochemical Testing Follow-up Biochemical Testing Collection and Storage of Plasma and Urine Specimens Interferences from Diet and Drugs Pharmacologic Tests Additional Interpretative Considerations Summary 91 8 Current trends in localization of pheochromocytoma Anatomical Imaging of Pheochromocytoma Computed Tomography Magnetic Resonance Imaging Functional Imaging of Pheochromocytoma MIBG Scintigraphy Positron Emission Tomography Somatostatin Receptor Scintigraphy (Octreoscan) Current Imaging Algorithm Treatment of pheochromocytoma Medical Therapy and Preparation for Surgery Postoperative Management Future trends and perspectives Genomics in Pheochromocytoma Research Proteomics in Pheochromocytoma Research Future Therapeutic Modalities for Pheochromocytoma 118 References 120 Index 167
9 To our children Tomáš, Ruud, Koen, Anne, and Suzanne
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11 The glory of medicine is that it is constantly moving forward, that there is always more to learn. Dr. William J. Mayo, 1928
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13 CHAPTER 1 Introduction Pheochromocytomas are rare but treacherous catecholamine-producing tumors, which if missed or not properly treated, will almost invariably prove fatal [1 6]. Prompt diagnosis is, therefore, essential for effective treatment, usually by surgical resection. The manifestations are diverse and the tumor can mimic a variety of conditions, often resulting in erroneous and delayed diagnosis [1, 7]. Therefore, not surprisingly pheochromocytoma earned the title great mimic [8]. The incidence of pheochromocytoma in autopsy studies is about % [9 14]. Autopsy studies have also shown that up to 50% of pheochromocytomas are unrecognized [12, 14]. Recent advances in biochemical diagnosis (the measurement of plasma free metanephrines), tumor localization (the use of positron emission tomography), surgical approaches (the use of laparoscopic adrenal-sparing surgery), and improved understanding of the pathophysiology and genetics of pheochromocytoma (the role of succinate dehydrogenase gene family or hypoxia and apoptosis pathways) are leading to earlier diagnosis and changes in management strategies and therapeutic options [1, 2, 5, 15 29]. Pheochromocytomas are most frequent in individuals between 40 and 50 years, with very slight predilection in females. The tumors occur in all races, but have been predominantly reported in caucasians [30]. Pheochromocytomas typically derive in about 85% of cases from adrenal medullary chromaffin tissue and in about 15% of cases from extra-adrenal chromaffin tissue [31]. Those arising from extra-adrenal tissue are commonly known as paragangliomas. The 2004 WHO classification of endocrine tumors defines pheochromocytoma as a tumor arising from catecholamine-producing chromaffin cells in the adrenal medulla an intra-adrenal paraganglioma. Paragangliomas are divided into two groups: those that arise from parasympathetic-associated tissues (most commonly along cranial and vagus nerves; e.g. glomus or carotid body tumors) and those that arise from sympathetic-associated chromaffin tissue (often designated extra-adrenal pheochromocytomas). Extra-adrenal pheochromocytomas arise mainly from chromaffin tissue of sympathetic ganglia in the abdomen (in about 75%) [32, 33]. Extra-adrenal pheochromocytomas in the abdomen most commonly arise from a collection 1
14 2 Chapter 1 of chromaffin tissue around the origin of the inferior mesenteric artery (the organ of Zuckerkandl) or aortic bifurcation [1]. Both adrenal and extra-adrenal paragangliomas display similar histopathological characteristics. Less frequent sites of pheochromocytoma include kidney, urethra, prostate, spermatic cord, genital tract, and liver. Most pheochromocytomas arise sporadically, but based on recent reports up to 24% are familial [25, 34]. Up to 25% of patients with pheochromocytoma present with adrenal incidentaloma, whereas approximately 5% are diagnosed at surgery [22, 35 39]. In contrast to sporadic pheochromocytomas that are usually unifocal and unilateral, familial pheochromocytomas are often multifocal and bilateral [1, 4, 7, 15, 40]. Although metastases may be rare for adrenal (about 10%) and familial (less than 5%; except succinate dehydrogenase subunit B SDHB pheochromocytomas [32, 41], the prevalence is up to 36% for extra-adrenal abdominal pheochromocytomas [38, 40, 42 44]. Finally, up to 14% of intra-adrenal pheochromocytomas show local recurrence [22, 30, 45]. One study also showed that patients with mainly adrenal pheochromocytoma have an increased risk for developing other cancers (e.g. liver and biliary tract cancers, malignant melanoma, cervix carcinoma, and central nervous tumors) [46]. According to different reviews and statistics, pheochromocytomas account for approximately % of patients with any degree of sustained hypertension [1, 15, 47 49]. However, this probably accounts for only 50% of persons harboring the tumor, when it is considered that about half the patients with pheochromocytoma have only paroxysmal hypertension or are normotensive. Also, despite the low incidence of pheochromocytoma among patients with sustained hypertension, it must also be considered that the current prevalence of sustained hypertension in the adult population of Western countries is up to 30% [50 52]. Thus, the prevalence of pheochromocytoma can be estimated to lie between 1:4500 and 1:1700, with an annual incidence of detection three to eight cases per 1 million per year in the general population [53].
15 CHAPTER 2 Historical comments Alfred Kohn, Professor of Histology at the Charles University in Prague, introduced the terms chromaffin, chromaffin system, paraganglion, and paraganglionic cell [54 58]. The name pheochromocytoma was proposed by Pick in 1912 [59] and comes from the Greek words phaios, dusky (brown), and chroma, color, and refers to the staining that occurs when the tumors are treated with chromium salts. The brown pigment of the chromaffin reaction is composed of oxidation products of epinephrine (adrenaline) or norepinephrine (noradrenaline) resulting in the generation of adrenochrome and noradrenochrome, respectively. The first diagnosis of pheochromocytoma was made in 1886 by Fränkel [60] who found bilateral tumors of the adrenal gland at autopsy in an 18-year-old girl who had died suddenly after collapse. Extraadrenal pheochromocytoma was first reported by Alezais and Peyron in 1908 [61]. Based on these findings they applied the term paraganglioma to describe the presence of extra-adrenal tumors arising in paraganglia. The first successful surgical removals of pheochromocytomas were by Roux in Switzerland in 1926 and by Mayo in the United States in 1927 [47, 62]. In 1936, epinephrine was isolated from a pheochromocytoma by Kelly et al. [63] but, it was not until 1946, that von Euler and his co-workers, and 1947, that Holtz and his co-workers reported independently the occurrence of norepinephrine in the body [64 66]. In 1949, Holton [67] first demonstrated the presence of norepinephrine in a pheochromocytoma. Early in the 1950s, von Euler showed that patients with pheochromocytoma had increased urine excretion of epinephrine, norepinephrine, or hydroxytyramine (metabolite of dopamine) [68]. Shortly thereafter, Lund together with Moller described elevated plasma concentrations of norepinephrine and epinephrine in patients with pheochromocytoma [69, 70]. In the late 1950s, Armstrong and co-workers were first in showing elevated urine excretion of vanillylmandelic acid in patients with pheochromocytoma [71]. In 1957, Axelrod and co-workers described O-methylation as the important pathways in catecholamine metabolism [72] and LaBrosse and co-workers for the first time demonstrated elevated urine excretion of normetanephrine (O-methylated metabolite of norepinephrine) in patients with pheochromocytoma [73]. 3
16 CHAPTER 3 Pathology Sporadic pheochromocytomas are generally solitary, well-circumscribed, encapsulated tumors with characteristic histopathological features [74, 75] (Figure 3.1). They are usually located in the adrenal gland or in its immediate vicinity (Figure 3.2). However, the adrenal gland may not be in its expected place atop the kidney, but actually located anywhere superior, inferior, medial, lateral, dorsal, or ventral to the kidney. Thus, pheochromocytoma may still be considered intra-adrenal in origin, if the cortex of the adrenal is found in close relationship to the pheochromocytoma. Malignant tumors appear to be larger, contain more necrotic tissue, and are composed of smaller cells than benign adrenal pheochromocytomas [47, 76, 77]. However, it is impossible Figure 3.1 Histopathology of sporadic pheochromocytoma (H&E, original magnification: 20 ) that shows characteristic nests of pheochromocytoma cells with abundant, finely granular basophilic cytoplasm and vesicular nuclei with nucleoli. High vascularity of pheochromocytoma is reflected in the prominent capillary network (gray) seen throughout the tumor. Cytoplasm can also be amphophilic or eosinophilic and nuclei can vary in size and shape (not shown). 4
17 Pathology 5 to distinguish malignant from benign pheochromocytoma based on histopathological features, although capsular invasion, vascular penetration, the presence of atypical nuclei, pleomorphism, higher mitotic count, and mitosis exist in both types of pheochromocytoma; they are more common in malignant pheochromocytoma [74, 77 79]. The presence of metastatic lesions where chromaffin cells are normally absent (e.g. in liver, lungs, lymphatic nodes, and bones) are currently consistent with the diagnosis of malignant pheochromocytoma [47, 75, 80]. As described by Linnoila et al. [43] fewer neuropeptides are expressed in malignant than in benign pheochromocytoma cells. There are no differences in immunohistochemical expression of cathepsins, basic fibroblastic growth factor, c-met, collagenase between benign and malignant pheochromocytomas [81]. Clarke et al. [81] reported that MIB-1 appears to be a good indicator of metastatic pheochromocytoma s potential with a specificity of 100% and a sensitivity of 50%. Recently, it has been shown that both telomerase activity and the catalytic subunit of telomerase (htert) are up-regulated in malignant, but not in benign pheochromocytomas [82, 83]. Currently, two scales are used to attempt to distinguish benign from malignant pheochromocytoma. The first one represents the so-called pheochromocytoma of the adrenal gland scaled score (PASS) [84] and the other one is based on the presence of immunohistochemical markers [85] (Tables 3.1 and 3.2). A PASS of 4 has been suggested to identify tumors that are histologically malignant. However, about 1/3 of patients with identified primary malignant tumors using a PASS score do not develop metastatic lesions although all patients in whom metastatic tumors are found, a PASS score of these tumors is 4. Widespread application of these scores with appropriate clinical follow-up in large prospective studies is needed to further validate these findings. Thus, there is currently no consensus on adoption of a formal scoring system; however, it is recommended that pathology Figure 3.2 A small intra-adrenal pheochromocytoma.
18 6 Chapter 3 Table 3.1 Pheochromocytoma of the adrenal gland scoring scale Feature Score if Present (Number of Points) Large nests or diffuse growth ( 10% of tumor volume) 2 Central (middle of large nests) or confluent tumor necrosis (not degenerative change) 2 High cellularity 2 Cellular monotony 2 Tumor cell spindling (even if focal) 2 Mitotic figures 3/10 HPF 2 Atypical mitotic figure(s) 2 Extension into adipose tissue 2 Vascular invasion 1 Capsular invasion 1 Profound nuclear pleomorphism 1 Nuclear hyperchromasia 1 Total score 20 HPF: high-power field. Adapted from Thompson [84]. Table 3.2 Immunohistochemical markers that may facilitate the evaluation of malignancy in pheochromocytomas Marker Expression in Malignant Pheochromocytoma Ki-67/Mib-1 Increases c-erbb-2 Increases No difference Inhibin βb Decreases p53 Increases No difference bcl-2 Increases No difference VEGF Increases Heparanase-1 Increases Tenascin Increases COX-2 Increases S-100 Decreases VEGF: vascular endothelial growth factor; COX-2: cyclooxygenase-2. Adapted from Salmenkivi [85]. reports conform to templates for minimal standard reporting endorsed by several pathology associations. The templates list the major elements of the proposed scoring systems and permit additional optional elements. The listing of potentially unfavorable findings will presumably flag a tumor for some type of follow-up, but the nature of the required follow-up remains unclear [86]. The most important immunohistochemical markers that facilitate the evaluation
19 Pathology 7 (a) (b) Figure 3.3 Electron microscopy shows the presence of membrane-bound, dense-core, neurosecretory epinephrine (E)- and norepinephrine (NE)-containing granules in (a) multiple endocrine neoplasia type 2 (MEN-2)- and (b) von Hippel Lindau (VHL)- associated pheochromocytoma. of malignancy in pheochromocytomas as introduced by Salmenkivi [85] are outlined in Table 3.2. Most pheochromocytomas range in size from 3 to 5cm [47, 74, 87]. Those that are larger than 5cm have a higher potential to metastasize [40, 88, 89]. The chromaffin reaction, originally described by Henle in 1865, is a deepbrown color of the adrenal medulla that occurs after the tissue is placed in a dichromate solution [90]. The reaction is due to the oxidation of the catecholamines, epinephrine and norepinephrine, into adrenochrome pigments. When this pattern is well developed it mimics tumor cell nests or zellballen, seen also in parasympathetic paragangliomas in the head and neck. Another pattern consists of anastomosing cords of cells (trabecular). The third and most common pattern is a mixture of anastomosing cell cords and nests of cells (Figure 3.1) [74]. The tumor cells are usually polygonal with an intermediate amount of lightly colored eosinophilic granular cytoplasm. Cells may vary in size from small to large [91]. Nuclei are well demarcated and generally eccentric in location. Nuclear pleomorphism with enlargement and hyperchromatism may be seen [74], this is not diagnostic of malignancy. Occasionally, tumor cells resemble ganglion cells with rounded, eccentric nuclei, and prominent nucleoli. Electron microscopy reveals the presence of membrane-bound, densecore, neurosecretory epinephrine- and norepinephrine-containing granules nm in diameter (Figure 3.3) [74]. In most tumors, the predominant granule is the one associated with norepinephrine, while in the normal gland the predominant granule is the one associated with epinephrine [92]. Chromaffin cells have ability to synthesize and secrete various amines and certain hormones, that is adrenocorticotropic hormone (ACTH), chromogranins, neuropeptide Y, calcitonin, angiotensin-converting enzyme, renin, vasoactive intestinal polypeptide, adrenomedullin, renin, atrial natriuretic factor, angiotensin-converting enzyme, thyrotropin-releasing hormone, parathormone, insulin, gastrin, melatonin, galanin, bombesin, opioids, synaptophysin, and others have also been found in neuroendocrine neoplasms, including pheochromocytoma [93 100].
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Pheochromocytoma This page intentionally left blank Pheochromocytoma Diagnosis, Localization, and Treatment Karel Pacak, MD, PhD, DSc National Institute of Child Health and Human Development NIH, Bethesda,
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