1485Vol. 11 | No. 02 | March- April 2014 |U R O LO G Y J O U R N A L Adrenal Ganglioneuromas: Experience from a Retrospective Study in a Chinese Population Liping Li,1,2 Jialiang Shao,1 Jianjun Gu,3 Xiang Wang,1 Lianxi Qu1,3 Corresponding Author: Lianxi Qu, MD Department of Urology, Huashan Hospital of Fudan University, 12 Wulumuqi Middle Road, Shanghai 200040, China. Tel: +86 21 5288 7080 Fax: +86 21 5288 8279 E-mail: qulianxi@medmail.com.cn Received November 2012 Accepted April 2013 1 Department of Urology, Huashan Hospital of Fudan University, Shanghai 200040, China. 2 Department of Urology, Zhongshan Hospital of Fudan University, Shanghai 200032, China. 3 Department of Urology, Nanhui Branch of Huashan Hospital, Fudan University, Shanghai 201300, China. Purpose:‎Ganglioneuromas‎(GNs)‎are‎benign‎neoplasms‎of‎combined‎neural‎crest,‎schwann- ian,‎and‎connective‎tissue‎origin,‎occurring‎rarely‎in‎the‎adrenal‎glands.‎The‎present‎study‎is‎ to‎share‎our‎experience‎regarding‎diagnostic‎and‎therapeutic‎management‎of‎these‎tumors.‎ Materials and Methods:‎Adrenal‎GNs‎of‎15‎patients‎were‎found‎incidentally‎with‎ultrasonog- raphy‎and‎were‎evaluated‎subsequently‎with‎computed‎tomography‎(CT)‎scan.‎Clinical‎data‎ as‎well‎as‎follow-up‎data‎were‎collected‎retrospectively.‎All‎the‎patients‎received‎operative‎ resection. Results:‎The‎mean‎age‎of‎the‎patients‎was‎38.4‎years‎(range,‎25-52‎years;‎male‎to‎female‎ra- tio,‎2:1).‎Of‎study‎subjects‎11‎patients‎had‎unilateral‎GN‎on‎the‎right‎side,‎and‎the‎remaining‎ 4‎on‎the‎left‎side.‎All‎but‎1‎patient‎were‎asymptomatic.‎No‎hormonal‎secretion‎was‎apparent.‎ Mean‎size‎of‎the‎tumors‎in‎CT‎scan‎was‎6.27‎cm‎(range,‎2.5-14‎cm),‎while‎10‎were‎larger‎ than‎5‎cm.‎Eight‎patients‎underwent‎open‎adrenalectomy‎and‎the‎remaining‎7‎underwent‎ laparoscopic‎anterior‎adrenalectomy.‎Histologically,‎all‎15‎neoplasms‎were‎completely‎dif- ferentiated,‎mature‎GN.‎We‎had‎no‎mortality‎or‎significant‎morbidity.‎Mean‎duration‎of‎hos- pitalization‎was‎5.5‎days‎(range,‎3-7‎days).‎There‎was‎no‎recurrence,‎during‎a‎mean‎follow- up‎of‎5.4‎years‎(range,‎1-10‎years).‎ Conclusion:‎Pre-operative‎diagnosis‎of‎adrenal‎GNs‎remains‎difficult‎merely‎according‎to‎ physical‎examination.‎Therefore,‎we‎recommend‎complete‎operative‎resection‎once‎malig- nancy‎cannot‎be‎excluded‎by‎pre-operative‎analyses.‎Laparoscopic‎adrenalectomy‎is‎a‎rea- sonable‎option,‎at‎least‎for‎tumors‎≤‎5‎cm. Keywords:‎adrenal‎gland‎neoplasms;‎ganglioneuroma;‎pathology;‎diagnosis;‎humans. MISCELLANEOUS 1486 | INTRODUCTION Ganglioneuromas‎(GNs)‎are‎benign‎neoplasms‎mainly‎originating‎from‎retroperitoneum‎and‎posterior‎medi-astinum‎and‎less‎frequently‎in‎the‎adrenals,‎and‎are‎ considered‎to‎occur‎more‎frequently‎in‎children‎or‎young‎adults. (1-6)‎ Clinically,‎ adrenal‎ ganglioneuromas,‎ usually‎ hormonally‎ non-secreting,‎ may‎ be‎ often‎ incidentally‎ found‎ in‎ radiologic‎ finding‎without‎any‎symptoms‎or‎present‎secondary‎to‎pressure‎ effects‎on‎adjacent‎structures.‎Therefore,‎the‎size‎of‎adrenal‎GNs‎ is‎larger‎than‎those‎of‎their‎more‎common‎counterparts‎in‎the‎ posterior‎mediastinum.(7-9)‎The‎aim‎of‎this‎study‎is‎to‎share‎our‎ experience‎regarding‎delineate‎the‎clinical‎course,‎diagnostic‎im- aging,‎and‎operative‎treatment‎of‎primary‎adrenal‎ganglioneuro- mas‎in‎adults‎in‎China. MATERIALS AND METHODS Between‎June‎1997‎and‎June‎2011,‎a‎total‎of‎15‎patients‎with‎ histologically‎proven‎adrenal‎incidentalomas‎were‎admitted‎to‎ Department‎of‎Urology‎in‎Huashan‎Hospital‎and‎ its‎Nanhui‎ Branch‎ of‎ Fudan‎ University,‎ Shanghai,‎ China‎ (Table).‎Their‎ clinical‎data‎were‎collected‎retrospectively,‎as‎well‎as‎follow- up‎data.‎All‎the‎patients‎were‎found‎with‎ultrasonography‎and‎ were‎evaluated‎subsequently‎with‎computed‎tomography‎(CT)‎ scan.‎To‎evaluate‎the‎functional‎status‎of‎the‎adrenal‎tumors,‎bio- chemical‎and‎hormonal‎screening‎was‎carried‎out‎in‎all‎patients.‎ The‎study‎protocol‎involving‎human‎materials‎were‎approved‎ by‎the‎Institutional‎Ethic‎Committee‎of‎Huashan‎Hospital‎and‎ its‎Nanhui‎Branch. RESULTS Clinical Findings The‎mean‎age‎of‎the‎patients‎was‎38.4‎years‎(range,‎25-52‎years;‎ male‎to‎female‎ratio,‎2:1).‎All‎but‎1‎patient‎were‎asymptomatic.‎ As‎shown‎in‎the‎Table,‎patient‎4‎had‎complaints‎of‎atypical‎up- per‎abdominal‎pain‎and‎a‎14-cm‎adrenal‎mass‎was‎found‎during‎ ultrasonographic‎investigation.‎No‎hormonal‎secretion‎was‎ap- parent.‎Hormonal‎evaluation‎revealed‎that‎catecholamine‎level‎ was‎within‎the‎normal‎range‎in‎all‎cases.‎All‎the‎15‎cases‎in‎our‎ series‎had‎normokalemia. Imaging Findings All‎neoplasms‎were‎reported‎as‎unilateral‎adrenal‎lesions‎and‎ seven‎of‎ten‎were‎right‎sided‎in‎CT‎scan.‎Mean‎size‎was‎6.27‎cm‎ (range,‎2.5-14‎cm),‎while‎10‎were‎larger‎than‎5‎cm‎(Table).‎All‎ cases had a solid appearance and low unenhanced attenuation value,‎up‎to‎30‎Hounsfield‎units‎(HU).‎Contrast‎enhanced‎CT‎ scan‎showed‎increased‎attenuation‎of‎40‎HU‎in‎1.‎Masses‎sur- round‎but‎not‎infiltrate‎main‎aortas‎and/or‎vein‎in‎CT‎scan‎and‎ arteriography‎(patient‎4;‎Figures‎1,‎A,‎B,‎C‎and‎D).‎None‎was‎ shown‎with‎calcification.‎Arteriography‎in‎this‎patient‎showed‎ that‎the‎mass‎did‎not‎invade‎the‎kidney‎artery.‎The‎remaining‎ neoplasms‎were‎homogeneous.‎CT‎scan‎showed‎evidences‎nei- ther‎of‎surrounding‎tissue‎infiltration‎nor‎regional‎lymph‎node‎ enlargement. Treatment All‎patients‎underwent‎complete‎resections,‎8‎open‎and‎7‎lapa- roscopic‎adrenalectomies.‎Mean‎operative‎time‎of‎open‎proce- dures‎was‎90‎min‎(range,‎65-150‎min).‎All‎laparoscopies‎were‎ completed‎ without‎ conversion.‎ Mean‎ laparoscopic‎ operative‎ time‎was‎104‎min‎(range,‎70-200‎min). There‎was‎no‎mortality,‎minor‎morbidity‎or‎complications‎in‎our‎ patients.‎No‎patient‎needed‎blood‎transfusion.‎Mean‎duration‎ of‎hospitalization‎was‎5.5‎days‎(range,‎3-7‎days).‎There‎was‎no‎ recurrence,‎during‎a‎mean‎follow-up‎of‎5.4‎years‎(range,‎1-10‎ years).‎The‎abdominal‎pain‎of‎patient‎4‎was‎relieved‎after‎the‎ad- renalectomy.‎In‎the‎procedure‎of‎patient‎4,‎the‎tumor‎was‎found‎ to‎conglutinate‎with‎posterior‎wall‎of‎inferior‎vena‎cava,‎upper‎ pole‎of‎right‎kidney,‎right‎erector‎spinae‎and‎part‎of‎the‎liver.‎ After‎complete‎resection‎of‎the‎mass,‎regional‎lymph‎node‎be- tween‎inferior‎vena‎cava‎and‎aorta‎was‎found‎to‎be‎enlargement‎ and‎gather‎into‎a‎mass.‎It‎was‎impossible‎to‎completely‎separate‎ the‎lymph‎node‎from‎the‎vein.‎Therefore,‎one‎lymph‎node‎was‎ removed‎to‎histopathology.‎No‎blood‎pressure‎fluctuation‎was‎ found‎in‎all‎the‎surgery‎procedures. Histopathology Mean‎tumor‎size‎on‎pathologic‎examination‎was‎6.93‎cm‎(range,‎ 3-15‎cm)‎on‎maximum‎diameter,‎while‎the‎mean‎radiologic‎pre- operative‎size‎of‎6.27‎cm.‎All‎tumors‎were‎nodular‎and‎well‎ encapsulated.‎The‎cut‎surface‎was‎stramineous‎in‎6‎cases‎and‎ tan-white‎in‎9‎cases.‎Eight‎tumors‎were‎hard‎as‎rubber;‎the‎re- maining‎two‎tumors‎were‎soft.‎Microscopically,‎all‎neoplasms‎ consisted‎of‎fascicles‎of‎Schwann-like‎cells‎and‎dispersed‎ma- ture‎ganglion‎cells‎(Figure‎2).‎No‎neoplasm‎showed‎immature‎ neuroblastic‎cells‎or‎areas‎of‎pheochromocytoma.‎No‎calcifica- tions‎were‎found. In‎patient‎4,‎the‎neoplasm‎macroscopically‎seemed‎to‎destruct‎ the‎surrounding‎gland‎(Figure‎3).‎One‎lymph‎node‎was‎removed‎ from‎that‎patient‎and‎the‎histopathology‎showed‎mature‎gangli- Miscellaneous 1487Vol. 11 | No. 02 | March- April 2014 |U R O LO G Y J O U R N A L Adrenal Ganglioneuromas | Li et al on‎cells.‎Immunohistochemistry‎was‎employed‎in‎patients‎3‎and‎ 4,‎showing‎positive‎staining‎of‎ganglion‎cells‎for‎neuron-specific‎ enolase‎(NSE)‎(Figure‎4),‎synaptophysin‎and‎positive‎staining‎of‎ Schwann‎cell-specific‎marker‎(S100)‎(Figure‎5).‎ DISSCUSSION Neoplasms‎of‎ganglion‎cell‎origin‎include‎neuroblastomas,‎gan- glioneuroblastomas,‎and‎GNS,‎among‎which‎GNs‎are‎benign‎ neoplasms‎of‎combined‎neural‎crest,‎schwannian,‎and‎connec- tive‎tissue‎origin.‎GNs‎are‎considered‎to‎occur‎more‎frequently‎ in‎children‎or‎young‎adults.‎The‎largest‎series‎of‎primary‎GNs‎ came‎from‎the‎Enzinger‎and‎colleagues,‎where‎42%‎of‎their‎pa- tients‎were‎less‎than‎20‎years‎old‎in‎a‎series‎of‎88‎GN‎patients. (1)‎Other‎studies‎also‎had‎similar‎results.(2-6)‎However,‎only‎20%‎ (3/15)‎were‎≤‎30‎years‎old‎(mean,‎38.4‎years)‎in‎our‎series,‎which‎ is‎concordant‎with‎other‎studies‎where‎the‎mean‎age‎at‎diagnosis‎ to‎be‎around‎39‎to‎50‎years.(8-10)‎In‎fact,‎this‎adrenal‎pathology‎ can‎affect‎all‎age‎groups,‎including‎older‎patients,‎because‎GN‎ patients‎are‎usually‎asymptomatic‎and‎without‎physical‎exami- nations‎it‎is‎difficult‎to‎find‎GNs‎for‎other‎medical‎problems.‎Oc- casionally‎GNs‎may‎produce‎nonspecific,‎mass-related‎symp- toms,‎as‎in‎patient‎4.‎GNs‎may‎secrete‎catecholamine‎often‎in‎ pediatric‎ganglioneuromas‎and‎neuroblastomas,(4,11) but rarely in mature‎GNs,(8-10,12)‎which‎is‎consistent‎with‎our‎findings. Radiologic‎diagnosis‎of‎adrenal‎GN‎on‎CT‎scan‎have‎been‎well‎ described that low attenuated ( non-enhanced attenuation below 40‎ HU‎ ),‎ homogeneous‎ masses‎ which‎ demonstrate‎ slight‎ to‎ moderate‎enhancement,(5,6,10)‎and‎often‎surround‎but‎not‎infil- trate‎main‎aortas‎and/or‎vein.‎Our‎series‎also‎showed‎this‎feature‎ even‎in‎arteriography.‎Approximate‎2.4‎to‎60%‎of‎GN‎cases‎with‎ calcifications‎have‎been‎reported‎in‎the‎literatures.(13-15) In our series,‎there‎was‎no‎calcification.‎ It‎is‎reported‎that‎radiologic‎findings‎are‎apt‎to‎underestimate‎ tumor‎size.‎In‎our‎series,‎the‎mean‎radiologic‎size‎was‎6.27‎cm,‎ while‎the‎mean‎histologic‎size‎was‎6.93‎cm.‎Tumor‎size‎>‎5‎cm,‎ heterogeneity,‎and‎calcifications‎are‎considered‎to‎be‎radiologic‎ signs‎indicating‎malignant‎adrenal‎tumor.‎The‎largest‎tumor‎of‎ our‎series‎was‎measured‎14‎cm,‎and‎resected‎by‎open,‎transab- dominal‎adrenalectomy‎due‎to‎the‎suspicion‎of‎cancer.(16-19) However,‎many‎aggressive‎ tumors‎share‎ these‎ features.‎Pre- Table. Clinical and imaging features of the series. Patient Gender Age (years) Symptom CT Size Pre Con- trast HU Post Con- trast HU Functiona Status Surgical Technique Histological Size (cm) 1 F 45 None (cm) <30 <30 None Laparoscopic 3 2 M 30 None 2.5 <30 <30 None Laparoscopic 5 3 M 33 None 5 30 30 None Open anterior 14 4 M 25 Abdominal pain 12 <30 40 None Open anterior 15 5 F 41 None 14 <30 <30 None Laparoscopic 3 6 F 44 None 3 <30 <30 None Open anterior 8 7 M 49 None 7 <30 <30 None Open anterior 7 8 F 52 None 6.5 30 30 None Open anterior 8 9 M 29 None 8 <30 <30 None Laparoscopic 5 10 M 38 None 4.5 <30 <30 None Open anterior 5 11 M 31 None 5 <30 <30 None Laparoscopic 4 12 F 33 None 4 <30 <30 None Laparoscopic 4 13 M 45 None 3.5 <30 <30 None Laparoscopic 5 14 M 40 None 4 <30 <30 None Open anterior 9 15 M 41 None 8 <30 <30 None Open anterior 9 Keys: M, male; F, female; CT, computerized tomography; HU, Hounsfield Unit. 1488 | operative‎diagnosis‎of‎adrenal‎GNs‎remains‎difficult.‎The‎final‎ diagnosis‎depended‎on‎histopathology.‎Macroscopically,‎most‎ GNs‎are‎large,‎encapsulated‎masses‎of‎firm‎consistency‎with‎ a‎ solid,‎ homogenous,‎ grayish-white‎ cut‎ surface.‎ Microscopi- cally,‎GNs‎mainly‎consist‎of‎mature‎and‎maturing‎ganglions‎and‎ Schwann‎cells‎in‎our‎series.‎Our‎immunohistochemical‎analysis‎ showed‎that‎they‎were‎characterized‎by‎reactivity‎with‎S100‎and‎ neuronal‎markers‎such‎as‎NSE.(1,9,15) Fine‎needle‎aspiration‎biopsy‎(FNAB)‎in‎the‎diagnosis‎of‎adre- nal lesions has a long history,(20)‎however,‎insufficient‎material‎ for‎diagnosis‎and‎its‎complications‎restrict‎its‎application.(21-24) It is‎only‎suggested‎in‎doubted‎metastatic‎adrenal‎carcinoma.(25-27) No‎patient‎of‎our‎series‎was‎undergone‎FNAB.‎ When‎adrenal‎incidentalomas‎are‎found,‎complete‎resection‎is‎ Figure 1. (A) Computed tomography scan showing a right adrenal ganglioneuroma with postcontrast enhancement of 40 Hounsfield and surround the renal artery, (B) a right adrenal gan- glioneuroma pushing forward inferior vena cava, conglutinating with posterior wall of inferior vena cava and surrounding tissues, (C) the coronal computed tomography scan reconstruction showing a right kidney pushed downward and a vasa vasorum from abdominal aorta to tumor and (D) renal arteriography showing a vasa vasorum from abdominal aorta to tumor. Figure 2. Mixture of large mature ganglion cells and spindle- shaped Schwann like cells. Hematoxylin and eosin staining ×100, original magnification. Figure 3. The neoplasm macroscopically seemed to destruct the surrounding gland. Figure 4. Neuron-specific enolase positive ganglion cells, stained brown. Schwann-like cells are also weakly positive, while adrenal cortical cells are negative. 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Adrenal Ganglioneuromas | Li et al suggested‎if‎the‎size‎is‎more‎than‎4‎cm.(28-30)‎In‎our‎series,‎3‎pa- tients‎strongly‎requested‎to‎resect‎the‎tumors‎even‎when‎the‎size‎ was‎less‎than‎4‎cm.‎Prognosis‎of‎mature‎adrenal‎ganglioneuro- mas‎after‎surgery‎is‎terrific.‎All‎surgeries‎were‎carried‎out‎with‎ no‎mortality‎and‎minimal‎morbidity‎despite‎the‎large‎size‎of‎the‎ neoplasms.‎After‎a‎mean‎follow-up‎of‎5.4‎years‎(range,‎1-10‎ years),‎no‎recurrence‎was‎observed.‎In‎the‎procedure,‎complete‎ resection‎is‎recommended‎in‎case‎of‎malignant‎transformation‎ of‎adrenal‎GN.(31-33)‎ As‎ the‎ laparoscopic‎ approach‎ develops,‎ almost‎ all‎ adrenal‎ masses‎could‎be‎resected‎laparoscopically‎regardless‎of‎the‎size.‎ Recently,‎Zografoset‎and‎colleagues‎have‎succeeded‎to‎resect‎ large‎adrenal‎GN‎with‎the‎size‎up‎to‎13‎cm‎by‎transabdominal‎ laparoscope.(7) CONCLUSION Pre-operative‎diagnosis‎of‎adrenal‎GNs‎remains‎difficult;‎there- fore,‎we‎recommend‎complete‎operative‎resection‎once‎malig- nancy‎cannot‎be‎excluded‎by‎pre-operative‎investigations.‎To‎ weigh‎the‎pros‎and‎cons‎according‎to‎our‎experience,‎laparo- scopic‎adrenalectomy‎is‎a‎reasonable‎option,‎at‎least‎for‎tumors‎ ≤‎5‎cm. 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