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1 中華癌醫會誌 (J. Chinese Oncol. Soc.) 24(4), , 2008 Case Report preoperative clinical diagnosis of paraganglioma is seldom made unless there are overt symptoms related to excess secretion of catecholamine. CT, MRI, and radionuclide imaging are useful for localizing the tujournal homepage: Retroperitoneal Paraganglioma Chia-Chi Tsai, Jiunn-Chang Lin*, Wen-Ching Ko, Tsang-Pai Liu Division of General Surgery, Department of Surgery, Mackay Memorial Hospital, Taipei, Taiwan 病例報告 後腹腔副神經節瘤 Abstract. Paragangliomas, known as extra-adrenal pheochromocytomas, are rare neuroendocrine tumors. Paragangliomas can be found anywhere from the skull base to the floor of the pelvis in locations of sympathetic ganglia. The symptoms and signs are nonspecific and related to excess secretion of catecholamine. An accurate preoperative clinical diagnosis of paraganglioma is seldom made unless there are overt symptoms related to excess secretion of catecholamine. CT, MRI, and radionuclide imaging are useful for localizing the tumor. The organs of Zuckerkandl are the most common site of involvement. Herein, we report on a retroperitoneal paraganglioma located in the left para-aortic region that was excised completely. This case emphasizes that extra-adrenal paraganglioma should be taken into account in the differential diagnosis of retroperitoneal masses, particularly those adjoining the abdominal aorta. Surgery remains the mainstay of treatment. Chemotherapy and radiotherapy can be used for palliation of symptoms. Keywords : Paraganglioma, Pheochromocytoma, retroperitoneal space 蔡家騏林俊昌 * 柯文清劉滄柏 馬偕紀念醫院一般外科 中文摘要 副神經節瘤為罕見的源發於腎上腺外的嗜鉻細胞瘤, 上至頭頸部下至骨盆腔的神經節都有可能發生, 最好發於後腹腔緊鄰主動脈, 其臨床症狀非常多樣化且缺乏專一性, 除非表現有過多兒茶酚胺的症狀, 否則不易與後腹腔腫瘤作鑑別診斷 斷層掃描, 核磁共振, 及核醫影像檢查是常用的定位此腫瘤的影像診斷工具, 治療以手術切除為主, 化療及電療為輔, 本篇病例報告乙例罕見的後腹腔副神經節瘤, 強調患者有鄰近主動脈的後腹腔腫瘤, 副神經節瘤需列入鑑別診斷 關鍵字 : 副神經節瘤 嗜鉻細胞瘤 後腹腔 INTRODUCTION Paragangliomas are rare neuroendocrine tumors. The clinical manifestations are nonspecific and related to excess secretion of catecholamine. An accurate
2 C. C. Tsai et al./jcos 24(2008) mor. Of the paraganglionic tissue adjacent to the aorta, the organs of Zuckerkandl are the most common site of involvement. The proximity of paragangliomas to the aorta in all instances may be of some value in differentiating these tumors from other primary retroperitoneal tumors. Herein, we report on a retroperitoneal paraganglioma located in the left para-aortic region that was excised completely. This case emphasizes that extra-adrenal paraganglioma should be taken into account in the differential diagnosis of retroperitoneal masses, particularly those adjoining the abdominal aorta. CASE REPORT A 46-year-old man presented with left abdominal pain for two days. The pain was localized to the left abdomen, and it was dull, intermittent, and without radiation to back. Inspection and deep palpation of the abdomen revealed a painless nonmobile mass approximately 7 cm in diameter with poorly defined margins and a firm resilient consistency. He had a one-year history of hypertension, and his blood pressure was under control. No headache, cold sweating, paroxysmal palpitation or family history of malignancy was noted. Abdominal ultrasonography revealed a mass lesion located in the left abdomen. For further evaluation, computed tomography (CT) (Figure 1) was done and showed a large well-defined heterogeneous low density soft tissue mass (7.4x7.3x 8.8cm) in the left para-aortic retroperitoneal region. There was no apparent enlargement of the pelvic or para-aortic lymph nodes. Under the impression of retroperitoneal tumor of unknown nature, he received laparotomy. On exploration, a hypervascular, encap- *Corresponding author: Jiunn-Chang Lin M.D. * 通訊作者 : 林俊昌醫師 Tel: ext.2154 Fax: jiunn@ms1.mmh.org.tw sulated mass was found very close to the aorta (Figure 2). Severe hypertensive episodes occurred while mobilizing the tumor. After removal of the tumor, blood pressure returned to normal. Histology revealed nests (zellballen) of pleomorphic cells separated by a prominent fibrovascular stroma. A prominent microvascular network was present. The cells were strongly immunoreactive with chromogranin-a, synaptophysin, and neuron-specific enolase (NSE) and negative for cytokeratin. Mitotic figures were occasionally seen. Definitive vascular invasion was not identified. The tumor was well-circumscribed and had a thin capsule. The pathologic diagnosis was retroperitoneal paraganglioma. The postoperative course was uneventful. During the six-month postoperative follow-up at our out-patient department, elevated blood pressure was still noted. DISCUSSION Paragangliomas (also known as extra-adrenal pheochromocytomas) are rare neuroendocrine tumors. They are composed of chromaffin cells and can arise in any area of the body containing embryonic neural crest cells [1]. They are distributed throughout the body in 3 basic chains: branchiomeric, intravagal, and aortosympathetic (Table 1) [2]. Ninety percent of such neuroendocrine tumors are contained within the adrenal gland as pheochromocytomas, and the remaining 10% are located elsewhere along the sympathetic chain, including the skull base and neck (5% of cases), thorax (10%), aorta (75%), and bladder (10%) [3]. Men are affected more frequently than women, and most patients are between the ages of 30 and 45 years [4]. They may be associated with familial syndromes, including multiple endocrine neoplasia, von Hippel-Lindau disease, neurofibromatosis, and Carney s syndrome. In the inherited forms, most of them are bilateral [5]. As in our case, of the paraganglionic tissue adjacent to the aorta, the organs of Zuckerkandl are the most common site of involvement. The organs of
3 258 C. C. Tsai et al./jcos 24(2008) (a) (b) Figure 1. (a) Unenhanced abdominal CT scan demonstrates an 8x7-cm soft-tissue mass adjacent to the aorta. (b) Contrast-enhanced CT scan demonstrates prompt peripheral enhancement Zuckerkandl are located along the aorta, beginning cranial to the superior mesenteric artery or renal artery and extending to the level of aortic bifurcation or just beyond. The proximity of paragangliomas to the aorta in all instances may be of some value in differentiating these tumors from other primary retroperitoneal tumors. Tumor location away from the aorta should eliminate paragangliomas from the differential diagnosis [3,5]. The clinical manifestations are nonspecific and related to excess secretion of catecholamine. The symptoms and signs include paroxysmal or persistent hypertension, throbbing headache, diaphoresis, tremor, nausea, vomiting, constipation, chest or abdominal pain, visual disturbance, and postural hypotension [5, 6]. The classic triad of headache, palpitation and sweating in a hypertensive patient was found to have a sensitivity of 91% and specificity of 94%[7]. However, about 8% of patients may be completely asymptomatic[7]. Therefore, approximately 10% of pheochromocytomas and paragangliomas are discovered incidentally during imaging studies performed to evaluate patients for unrelated symptoms [8]. In our patient, hypertension persisted after operation. We suspect that the patient has concomitant essential hypertension. At gross examination, paragangliomas range from 1 to 6 cm in diameter, with malignant tumors tending to be slightly larger [9,10]. They are firm, encapsulated masses that adhere to adjacent structures. On cut section, paragangliomas are tan-red, with or without areas of necrosis. Microscopic analysis showed neuroendocrine cells arranged in clusters called zellballen and interspersed with fibrovascular stroma, which produced strong contrast enhancement in the CT or MRI imaging. Specific antibodies from neuroendocrine markers such as synaptophysin, chromogranin and S-100 protein can be used to confirm the diagnosis. There are no standardized histological criteria for differentiating malignant and benign paragangliomas and pheochromocytomas. Therefore, malignant tumors are diagnosed based on the presence of local invasion or distant metastasis [11]. For patients with symptoms related to excess catecholamine production, it is important to confirm or to exclude the presence of hyperactive catecholamine-secreting tumors by measuring catecholamines and their related metabolites in the plasma and urine. The available tests include plasma catecholamines, 24-hour urine fractioned metanephrines, 24-hour urine catecholamines, serum chromogranin-a, and plasma
4 C. C. Tsai et al./jcos 24(2008) Figure 2. Photography of the gross specimen shows a 9x 8-cm mass with hemorrhagic and necrotic areas free metanephrines. Of these parameters, plasma free medium injection. Because of the risk of a hyperten- metanephrines are considered the most sensitive [12]. sive crisis after intravenous injection of contrast me- However, no single analysis can achieve 100% accu- dium, it is a common policy at many institutions that racy because pheochromocytomas are a heterogeneous only non-enhanced CTs with per oral contrast medium group of hormone-secreting tumors. Care should be are done to rule out pheochromocytomas or paragan- taken when interpreting the results of these tests be- gliomas. On the other hand, enhanced CT scan is cause several medications and foodstuffs may produce helpful in detection of small tumors and detailed false-positive results, including the beta-blockers evaluation of local invasion. If enhanced CT is crucial, which may be prescribed for patients with presump- prophylaxis with alpha- and beta-blockers is recom- tive diagnosis of essential hypertension. mended as a safety measure. Biochemical confirmation of the diagnosis should MR imaging is considered a sensitive and safe be followed by radiologic evaluation to locate the tu- imaging modality for patients with pheochromocy- mor. Being familiar with the radiological findings and tomas or paragangliomas, especially when the tumors clinical characteristics are helpful in the differential are functional [5,14]. Multiplanar imaging also offers diagnosis of retroperitoneal tumors, including para- a more comprehensive demonstration of the relation- gangliomas and other neurogenic tumors, and in the ship between the tumors and adjacent structures such determination of the extent of tumor extension for ap- as the kidney, inferior vena cava, and aorta. In most propriate treatment planning. On CT images, there are cases, they are hypointense or isointense on no specific imaging findings for paragangliomas [13]. T1-weighted images (T1W1s), markedly hyperintense They are usually large tumors with areas of hemor- on T2-weighted images (T2W1s) and strongly en- rhage or necrosis and avid enhancement after contrast hanced after gadolinium injection. Markedly increased
5 260 C. C. Tsai et al./jcos 24(2008) Table 1. Distribution of the Paraganglia Branchiomeric chain Associated with parasympathetic nervous system; distributed along the jugular vein, vagus nerve, and larynx. Carotid bodies: components of the branchiomeric system, chemoreceptors that monitor blood levels of O2 and CO2. Intravagal chain Associated with parasympathetic nervous system; distributed along the vagus nerve. Aortosympathetic chain Associated with sympathetic nervous system; distributed along the abdominal aorta. Organs of Zuckerkandl: components of the aortosympathetic group located between the renal artery and the bifurcation of the aorta; first described by Emil Zuckerkandl in 1901 at the University of Vienna; probably serve to maintain fetal blood pressure in the early stages of fetal life; they undergo involution after the 8 th month of gestation. Visceral paraganglia Within the bladder and other organs. intensity on T2W1s may be essential for differential diagnosis of adrenal tumors because most other adrenal tumors tend to be isointense [15]. However, it should be kept in mind that a significant minority (up to 30%) of these tumors do not have such typical appearance. If no lesion can be found by CT or MRI in the setting of positive laboratory results, radionuclide imaging with metaiodobenzylguanidine (MIBG) or Indium-111 pentetreotide is suggested to search for occult lesions. Other indications for radionuclide imaging include locating multiple primary tumors, tumors outside the usual locations and metastases [5]. Positron emission tomography with 18F-fluorodeoxyglucose may also be useful in evaluating for metastatic disease, but larger clinical studies are still required before accurate comparisons can be made between positron emission tomography with 18Ffluorodeoxyglucos and MIBG scanning in terms of sensitivity and specificity [5]. Surgical removal of extra-adrenal paragangliomas may be accompanied by severe and acute hemodynamic changes. In a retrospective study, Kinney et al found that preoperative factors associated with adverse perioperative events included large tumor size, prolonged duration of anesthesia, and increased levels of preoperative urinary catecholamines and catecholamine metabolites [16]. In our patient, blood pressure fluctuation was most severe during manipulation of the tumor, which may be attributed to excessive catecholamine release secondary to its larger size, its more difficult resection and extensive manipulation. When a retroperitoneal tumor is discovered in a patient with pertinent symptoms and signs or hypertension, paraganglioma should be considered and preoperative screening is necessary. As soon as the biochemical diagnosis of paraganglioma has been confirmed, careful preoperative preparation is required including aggressive appropriate blood pressure control, sufficient planned operative time, collaborative operative support and sufficient blood-replacement products. Control of elevated blood pressure caused by elevated catecholamines in the preoperative period should include α- blockade and intravenous hydration, followed by β- blockade only after α- blockade had been optimized. When the hospital, patient and surgeon are adequately prepared, even very large tumors may be safely resected. Surgery remains the mainstay of treatment for all paragangliomas. Once the diagnosis of paraganglioma is made, every attempt should be made to perform a complete surgical resection. Resection offers the only chance of cure. In a series of 22 cases of extra-adrenal retroperitoneal paraganglioma from Memorial Sloan- Kettering Cancer Center, the 5-year survival for unre-
6 C. C. Tsai et al./jcos 24(2008) sected tumors was 19%, compared with 75% after complete resection [17]. Although % of paragangliomas are malignant, there are no reliable markers and histopathologic distinction between benign and malignant tumors. Malignancy only can be confirmed by the presence of distant metastasis or local recurrence. Once metastasis occurs, the prognosis is very poor with a 5-year survival of 20-45% [10,11]. Adjuvant therapies include chemotherapy, m-iodobenzylguanidine ( 131 I-MIBG) treatment and external radiotherapy, but there is no consensus concerning the optimal management of patients with malignant tumors. Most metastases occur within the first few years but may occur as late as 41 years after surgery [18]. Therefore, life-long follow-up of all patients with paragangliomas is necessary. Annual testing of 24-h urine excretion of metanephrines and catecholamines or periodic computerized imaging is mandatory. REFERENCES 1. Buonuomo V, Ruggiero A, Rando G, et al. Malignant retroperitoneal paraganglioma: case report and review of the literature. Pediatric Hematology & Oncology 21(8): 731-8, Tekautz TM, Pratt CB, Jenkins JJ, et al. Pediatric extraadrenal paraganglioma. J Pediatr Surg 38: , Whalen RK, Althausen AF, Daniels GH. Extraadrenal pheochromocytoma. J Urol 147: 1-10, Mikhail RA, Moore JB, Reed DN Jr, et al. Malignant retroperitoneal paragangliomas. J Surg Oncol 32: 32-36, Saurbon DP, Kruskal JB, Stillman IE, et al. Best case from the AFIP: Paraganglioma of the organs of Zuckerkandl. Radiographics 23: , Francis IR, Korobkin M. Pheochromocytoma. In: Pollack HM, McClennan BL, ed. Clinical urography, 2nd edition, Philadelphia: Saunders, pp , Bravo EL, Tagle R. Pheochromocytoma: state-ofthe-art and future propects. Endocr Rev 24: , Dunnick NR, Korobkin M. Imaging of adrenal incidentalomas: current status. AJR Am J Roentgenol 179: , Golstein RE, O neill JA, Holcomb GW 3rd, et al. Clinical experience over 48 years with pheochromocytoma. Ann Surg 229: , John H, Ziegler WH, Hauri D, et al. Pheochromocytoma: can malignant potential be predicted? Urology 53: , Edstrom Elder E, Hjelm Skog AL, Hoog A, et al. The management of benign and malignant pheochromocytoma and abdominal paraganglioma. Eur J Surg Oncol 29: , Lenders JW, Pacak K, Walther MM, et al. Biochemical diagnosis of pheochromocytoma: which test is best? JAMA 287: , Hayes WS, Davidson AJ, Grimley PM, et al. Extraadrenal retroperitoneal paraganglioma: clinical, pathologic, and CT findings. AJR Am J Roentgenol 155: , Falke TH, van Seters AP, Sandler MP. Magnetic resonance imaging of functioning paraganglioms. Magn Reson Q 6: 35-64, Bravo EL. Evolving concepts in the pathophysiology, diagnosis, and treatment of pheochromocytoma. Endocr Rev 15: , Kinney MAO, Warner ME, van Heerden JA, et al. Perianesthetic risk and outcomes of pheochromocytoma and paraganglioma resection. Anesth Analg 91: , Sclafani LM, Woodruff JM, Brennan MF. Extraadrenal retroperitoneal paragangliomas: Nature history and response to treatment. Surgery 108: , Proye CA, Vix M, Jansson S, et al. The pheochromocytoma: a benign, intra-adrenal, hypertensive, sporadic unilateral tumor. Does it exist? World J Surg 18: , 1994.
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