Pulmonary Resection for Metastatic Adrenocortical Carcinoma: The National Cancer Institute Experience

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1 Pulmonary Resection for Metastatic Adrenocortical Carcinoma: The National Cancer Institute Experience Clinton D. Kemp, MD,* R. Taylor Ripley, MD,* Aarti Mathur, MD, Seth M. Steinberg, PhD, Dao M. Nguyen, MD, Tito Fojo, MD, PhD, and David S. Schrump, MD, MBA Surgery Branch, Center for Cancer Research; Biostatistics and Data Management Section, Office of the Clinical Director, Center for Cancer Research; and Medical Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland GENERAL THORACIC Background. Adrenocortical carcinoma (ACC) is a rare neoplasm with a high propensity for locoregional recurrences and distant metastases for which there are no effective systemic therapies. This study was undertaken to determine outcomes of patients undergoing pulmonary metastasectomy for ACC. Methods. A single-institution retrospective review was performed of patients undergoing pulmonary metastasectomy for ACC from 1979 to Results. Twenty-six patients underwent 60 pulmonary metastasectomies. Fifteen patients (58%) underwent unilateral thoracotomy, 6 (23%) had staged thoracotomies, and 5 (19%) underwent median sternotomy as the initial thoracic procedure. Median number and size of lesions were 6 and 2 cm, respectively. Twenty-three patients (88%) were rendered free of disease in the lung, and 14 (54%) were rendered completely free of disease. Median overall and 5-year actuarial survivals from initial pulmonary metastasectomy were 40 months and 41%, respectively, with a median potential follow-up of 120 months. Median recurrence-free survival (RFS) and 5-year RFS for ipsilateral thoracic recurrences were 6 months, and 25%, respectively. The median RFS in the contralateral thorax was 5 months. Time to first recurrence after adrenalectomy and T stage of the primary tumor, but not adjuvant or neoadjuvant chemotherapy, were associated with increased overall survival after pulmonary metastasectomy. Conclusions. This study represents the most comprehensive review of outcomes of patients undergoing pulmonary metastasectomy for ACC. Given the lack of effective systemic therapies, pulmonary metastasectomy may be beneficial in properly selected patients. (Ann Thorac Surg 2011;92: ) 2011 by The Society of Thoracic Surgeons Adrenocortical carcinoma (ACC) is a rare neoplasm, accounting for 0.2% of all cancer deaths annually in the United States [1, 2]. Patients with ACC typically present with local symptoms referable to a large adrenal mass or systemic manifestations of hypercortisolism, virilization, feminization, or hyperaldosteronism. Most patients with ACC have advanced disease at diagnosis, and more than 25% present with distant metastases. Complete resection of the primary tumor is the most consistently cited prognostic factor for long-term survival in patients with localized ACC [3, 4]. The median and 5-year survivals of patients undergoing R0 resections are approximately 74 months, and 16% to 50%, respectively [4]. In contrast, median and 5-year survival rates for patients with incompletely resected primary tumors are 12 months, and 5%, respectively. Despite undergoing Accepted for publication May 2, *These authors contributed equally to this work. Presented at the Poster Session of the Forty-seventh Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31 Feb 2, Address correspondence to Dr Schrump, Section of Thoracic Oncology, Surgery Branch, National Cancer Institute, 10 Center Dr, Rm MSC 1201, Bethesda, MD ; david_schrump@nih.gov. complete resections, 70% to 85% of ACC patients develop locoregional recurrences or distant metastases, which are refractory to systemic therapies. The adrenolytic agent, mitotane (the most commonly used drug for ACC) has no clear benefit as adjuvant therapy in patients undergoing complete resections of their primary neoplasms [5 7]. In the palliative setting, mitotane mediates objective response rates of less than 20%, with virtually no complete responses in patients with inoperable primary ACC, locally recurrent, or metastatic disease [8]. The lack of effective chemotherapy has prompted evaluation of aggressive resections of locally recurrent or metastatic ACC, which most frequently involves the lungs and liver [3, 9, 10]. Similar to surgery for primary ACC, R0 resections for locoregional or systemic recurrences appear to be associated with improved survival; complete resection of metastatic disease is achieved more often than locoregional recurrences [3, 9, 10]. Although pulmonary metastasectomy for ACC has been described previously, published series have involved relatively few patients undergoing thoracic resections, and outcomes for these patients have not been analyzed separately from patients having resections at other sites; hence, the 2011 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur

2 GENERAL THORACIC 1196 KEMP ET AL Ann Thorac Surg PULMONARY METASTASECTOMY FOR ACC 2011;92: role of pulmonary metastasectomy for ACC has not been clearly established [11 13]. The present study was undertaken to examine outcomes of patients undergoing pulmonary metastasectomy for ACC in an attempt to identify prognostic factors that may guide future therapy of patients with these neoplasms. Patients and Methods Data Collection and Clinical Assessment A retrospective review was undertaken of patients undergoing pulmonary metastasectomy for ACC at the National Cancer Institute, Bethesda, MD, from 1979 through This study was approved by the Institutional Review Board and all patients were enrolled on approved research protocols, with written informed consent obtained prior to any interventions. Five of these patients were included in a report from 1991 [14]. Inclusion criteria were pathologically confirmed ACC from a resected lung lesion. Exclusion criteria were radiofrequency ablation or biopsy without resection of the lesion. Medical records were reviewed and analyzed in terms of patient demographics, Lee stage, tumor-nodes-metastasis stage, synchronous metastatic disease, functional status, neoadjuvant and adjuvant chemotherapy for the primary adrenalectomy and pulmonary metastasectomy, disease-free interval (DFI), staged procedures, postoperative no evidence of disease (NED) status, ipsilateral and contralateral NED status, and presence and resection of synchronous extrapulmonary disease. Table 1. Demographics Variable No. (%) Feature Age at primary adrenalectomy, years 37 (17 66) Age at lung operation, years 39 (18 68) Sex, M/F 7/19 Lee staging classification: II 6 (23) III 9 (35) IV 6 (23) Unknown 5 (19) Hormonal status at initial presentation: Unknown 5 (19) Nonfunctional 8 (31) Functional 15 (58) Hypercortisolism 10 (67) Hyperaldosteronism 2 (13) Virilization 1 (7) Feminization 2 (13) Disease status after primary adrenalectomy: No evidence of disease (NED) 20 (77) Patients resected to NED after primary adrenalectomy (n 20) Disease-free interval, median 17 months Systemic therapy: Adjuvant chemotherapy 7 (27) F female; M male; NED no evidence of disease. Statistical Analysis Overall survival (OS) was calculated from the date of pulmonary resection until the date of last encounter, or date of death, as appropriate. For patients resected to NED, disease-free survival (DFS) was calculated as the time from pulmonary resection until the first recurrence, or the last follow-up without a recurrence, as appropriate. Pulmonary recurrence-free survival (RFS) was calculated from the date of pulmonary resection until the date of death, last follow-up, or date of first recurrence in the lung after the date of the pulmonary resection. For patients with residual disease after the operation, progression-free survival (PFS) was calculated from the date of pulmonary resection until progression of disease at any site or the last follow-up without progression, as appropriate. The RFS and PFS were similarly calculated for recurrences in the ipsilateral and contralateral hemithoraces. Contralateral recurrences were calculated for patients who did not undergo bilateral metastasectomy through median sternotomy or staged thoracotomies. All staged procedures were performed within 2 months, and recurrences or progression were defined as new disease after the second thoracotomy. The probabilities of survival, lung RFS, DFS, or PFS were calculated by the Kaplan-Meier method; the statistical significance of the difference between pairs of Kaplan-Meier curves was determined by the log-rank test for cases in which the distinguishing characteristic of the curve was known at the date of resection. Clinicopathologic features were evaluated for their association with outcome by univariate methods described above. All p values are 2-tailed, and are presented without adjustment for multiple comparisons; a p value less than 0.05 was considered statistically significant. Results Patient Characteristics Twenty-six patients met criteria for analysis (Table 1). Twenty-one patients had their initial adrenalectomies prior to referral. Two patients had pulmonary metastases at diagnosis, neither of whom underwent synchronous resections. Median times to recurrence or progression at any site were 17 months and 11 months, respectively. All 23 patients with adequate data for assessment of chemotherapy response had progressive disease, with a median time to progression of 7 months. Operative Findings Twenty-six patients underwent pulmonary metastasectomy (Table 2). Eleven patients (42%) received neoadjuvant chemotherapy prior to pulmonary resection. Fifteen patients (58%) underwent unilateral thoracotomy, 6 (23%) had staged thoracotomies, and 5 (19%) underwent median sternotomy. A lobectomy was performed in 3 patients. Nonanatomic resections were performed in 23 patients. All but 1 of these procedures were open. Formal lymphadenectomy was not performed. The median number of

3 Ann Thorac Surg KEMP ET AL 2011;92: PULMONARY METASTASECTOMY FOR ACC Table 2. Operative Findings Operative Findings No. (%) Initial pulmonary resection: Unilateral thoracotomy 15 (58) Staged thoracotomies 6 (23) Median sternotomy 5 (19) Lobectomy (RML, RLL, LLL) 3 (12) Nonanatomic resection 23 (88) No. of thoracotomies: 1 16 (62) 2 a 3 (12) 3 3 (12) 5 1 (4) 6 3 (12) No. of pulmonary metastases: 1 7 (27) (15) (15) (23) (12) 34, 36 2 (8) Median (range) 4 (1 36) Synchronous extrapulmonary metastases: Extrapulmonary disease present 6 (23) Resection of extrapulmonary disease 2 Complete resection of extrapulmonary disease 1 Incomplete resection of extrapulmonary disease 1 Disease status after initial pulmonary resection: No. (%) or months NED 14 (54) NED ipsilateral lung b 23 (88) NED in contralateral lung c 21 (81%) Recurrence-free survival ipsilateral lung 7 Progression-free survival ipsilateral lung 4 Recurrence-free survival contralateral lung 10 Progression-free survival contralateral lung 2 Unilateral/bilateral initial pulmonary 10 (38)/16 (62) recurrence Systemic therapy: Neoadjuvant chemotherapy 11 (42) Adjuvant chemotherapy 11 (42) a Staged thoracotomy not included as second resection. b Includes both hemithoraces for staged thoracotomies and median sternotomy. c Fifteen patients did not have an operation in the contralateral lung. NED no evidence of disease; RML right middle lobectomy; RLL right lower lobectomy; LLL left lower lobectomy. lesions was 6 (range, 1 to 36). Detailed pathologic information was available for 23 patients (88%); the median and average diameters of the largest lesions were 2 cm and 3 cm (range, 0.7 to 6.5 cm), respectively. Margins were negative in all patients recorded. Ten patients (38%) were rendered completely NED after unilateral thoracotomy or sternotomy, and an additional 4 patients were rendered completely NED after staged thoracotomies; hence, (54%) patients were completely NED and 23 (88%) were NED in the lungs, but had residual extrathoracic disease after initial intended metastasectomy procedures. Twelve patients (46%) had residual disease; 9 of these patients were rendered NED in the chest after initial unilateral or planned bilateral metastasectomy procedures. Two had thoracic disease after median sternotomy, 1 had ipsilateral thoracic disease after unilateral thoracotomy, 5 had contralateral disease after unilateral thoracotomy, and 5 had residual extrathoracic disease with 1 patient having both intrathoracic and extrathoracic disease. Of the 26 patients, 16 (62%) had bilateral disease at presentation for metastasectomy; 11 patients were rendered NED in the chest after sternotomy (6 patients) or staged thoracotomies (5 patients). Five (19%) patients had residual contralateral disease. A contralateral thoracotomy was intended for 1, but was performed 6 months later; hence, this patient was not included in the staged thoracotomy group. Four patients had residual contralateral disease without intent to be addressed at initial thoracotomy due to low volume of disease. Six patients (23%) had synchronous extrathoracic disease. Four of these patients had hepatic disease, one had retroperitoneal disease and periportal lymph nodes, and 1 had retroperitoneal disease and a spinal metastasis. Two patients underwent synchronous lung and liver resections; 1 was rendered NED, and the other had complete resection of the liver disease but had residual pulmonary metastases after median sternotomy. Ten patients (38%) underwent 28 additional thoracotomies (Table 2). Nonanatomic resections were performed in all but 1. The median number of resected lesions was 4 (range, 1 to 36). The median and average sizes of the largest lesions were 2 cm and 2.3 cm (range, 0.7 to 4.5 cm), respectively. The margins were negative in all metastasectomy procedures, with 95% having pathology data adequate for analysis. No postoperative deaths were observed. Postoperative complications occurred in 12% of patients undergoing initial pulmonary metastasectomy procedures. The median blood loss was 125 ml (range, 50 to 1,400 ml); the 1,400 ml blood loss occurred in a patient undergoing pulmonary metastasectomy through median sternotomy with synchronous hepatic resection. Postoperative complications occurred in 18% of the 28 repeat metastasectomy procedures. Median blood loss from the reoperations was 100 ml (range, 50 to 1,000 ml). Clinical Outcomes and Prognostic Factors Although not used for prognostication, the median OS and 5-year actuarial survival from the adrenalectomy were 79 months and 63%, respectively, with a median potential follow-up of 165 months. Twelve patients survived longer than 5 years, 3 of whom died of disease. The median time to pulmonary disease after initial adrenalectomy was 11 months. Median overall and 5-year actuarial survivals for all 26 patients after initial pulmonary metastasectomy were 40 months and 41%, respectively (Fig 1A), with a median potential follow-up of 120 months. Four patients survived GENERAL THORACIC

4 GENERAL THORACIC 1198 KEMP ET AL Ann Thorac Surg PULMONARY METASTASECTOMY FOR ACC 2011;92: not undergo staged thoracotomies or median sternotomy, the combined median RFS-PFS in the contralateral thorax was 5 months. The median RFS in the contralateral chest for the 7 patients resected to NED was 10 months, whereas the PFS in the contralateral chest was 2 months for 8 patients not rendered NED. Prognostic factors for the initial pulmonary resection were evaluated for all 26 patients. Patients with times to progression or recurrence less than 17 months had median survivals of 25 months; in contrast, median survival had not been reached for patients with times to progression or recurrence greater than 17 months (p 0.015). Patients with T2 tumors had median survivals that had not been reached compared with 28 months for patients with T3/T4 tumors (p 0.024), respectively. There was a trend toward increased overall survival for those patients with a time to pulmonary disease greater than 11 months compared with those with a shorter pulmonary DFI (59 months versus 26 months; p 0.17). Factors that did not Fig 1. Survival of patients undergoing metastasectomy for adrenocortical carcinoma (ACC). (A) Overall survival of 26 patients undergoing pulmonary resection for ACC. (B) Disease-free survival after pulmonary resection for patients rendered no evidence of disease. longer than 5 years. The median DFS (includes extrathoracic disease) for patients resected to NED was 6 months (Fig 1B), whereas the median PFS for patients not resected to NED was 2 months. The median OS for the 15 patients who did not receive adjuvant chemotherapy had not been reached; median OS for the 11 patients who received adjuvant chemotherapy was 36 months (p 0.46). The recurrence of disease in ipsilateral and contralateral hemithoraces was examined separately. For patients who underwent staged thoracotomies or median sternotomies, disease in either hemithorax was considered ipsilateral recurrence. Contralateral recurrence and progression were recorded only for patients who underwent unilateral metastasectomy without staged procedures. For the 26 patients, combined median RFS and PFS and 5-year survivals for ipsilateral thoracic recurrences were 6 months and 25%, respectively (Fig 2A). The median DFS for patients resected to NED was 7 months (Fig 2B), whereas the median PFS for patients not resected to NED was 4 months. For the 15 patients who did Fig 2. Hemithoracic recurrences of adrenocortical carcinoma. (A) Combination of recurrence-free survival and progression-free survival in the ipsilateral chest for all 26 patients. Ipsilateral recurrences include both sides if the patient underwent bilateral thoracotomy or median sternotomy. (B) Ipsilateral recurrence-free survival for patients resected to no evidence of disease.

5 Ann Thorac Surg KEMP ET AL 2011;92: PULMONARY METASTASECTOMY FOR ACC influence survival included functional status of the primary neoplasm (p 0.23), adjuvant chemotherapy after adrenalectomy (p 0.91), pulmonary disease as the first metastatic site (p 0.93), resection to completely NED (p 0.94) or NED in the lungs (p 0.70) after initial pulmonary metastasectomy, neoadjuvant chemotherapy prior to pulmonary resection (p 0.15), staged procedure (p 0.61), and overall number of lesions (p 0.81). Factors associated with a trend for worse survival included presence of extra-adrenal disease at the time of primary adrenalectomy (29 months versus not reached; p 0.14), presence of contralateral pulmonary metastases (4 vs 6 months; p 0.15), and receiving adjuvant chemotherapy after pulmonary resection (3.7 vs 5.3 months; p 0.11). For the 10 patients who underwent a second thoracotomy, the median OS had not yet been reached and the 5-year actuarial survival was 57% after repeat resection. The median times to ipsilateral and contralateral recurrences were 11.8 months and not yet reached, respectively. No prognostic factors were evaluated for the second thoracotomy given the small number of patients. Comment Adrenocortical carcinoma is a relatively rare but lethal malignancy for which no effective systemic therapy regimens have been established. More than 50% of ACC patients present with stage III or stage IV disease. Fiveyear and median survivals for patients with stage I or II disease range from 45% to 60% and 60 to 100 months, respectively. In contrast, 5-year and median survivals for patients with stage III or stage IV disease range from 10% to 25%, and 5 to 18 months, respectively [15]. Nearly 40% of patients undergoing curative resection of ACC develop recurrent or metastatic disease, with median DFI of 21.7 months; nearly 50% of patients with metastatic disease have pulmonary metastases [9, 15]. Our analysis revealed a median time of 11 months from adrenalectomy to pulmonary metastases, possibly reflecting the relatively advanced nature of disease in patients referred to our institution for investigational therapy. Limited information is available regarding pulmonary metastasectomy for ACC. Schulick and Brennan [4] observed that the lungs were the most common sites of resection for 29 of 53 patients (55%) undergoing metastasectomy for ACC. Although survival of pulmonary metastasectomy patients was not provided in this report, a median survival of 16 months was noted for the 53 patients undergoing metastatic resections of all sites. Jensen and colleagues [14] reported the initial experience at our institution with 15 resections for metastatic ACC, which included 5 patients who had lung resections. The median survival time from diagnosis to first recurrence was 27 months; survival of patients undergoing pulmonary metastasectomy was not reported. Similarly, in the report by Crucitti and colleagues [9] pertaining to multiinstitutional management of 129 patients with advanced ACC over a 15-year period, therapeutic interventions and 1199 survivals of 5 patients who presented with pulmonary metastases, and 16 patients who developed pulmonary metastases after adrenalectomy, were not discussed. Icard and colleagues [16] reported the experience of the French Association of Endocrine Surgeons pertaining to multi-institutional management of 253 cases of ACC; despite 41.5% of patients having associated procedures including nephrectomy (29%), splenectomy (10%), hepatic resection (8%), and distal pancreatectomy (4%), no patients were reported to have had thoracic metastasectomies. After resection of recurrent or metastatic ACC, several factors have been reported to be associated with longterm survival. Crucitti and colleagues [9] reported mean survivals of 41.5 and 15.6 months, respectively (5-year: 48.2% vs 7%; p ), for patients who underwent resection of recurrent disease versus those who did not. Schulick and Brennan [4] determined that after resection of recurrent or metastatic ACC, disease-specific survival was significantly longer for patients who had complete resections versus those who did not (74 months versus 16 months, respectively; p 0.001). Jensen and colleagues [14] reported that a DFI greater than 12 months was associated with prolonged survival. The DFI greater than 9 months was associated with long-term survival of patients undergoing hepatic metastasectomy for ACC at the National Cancer Institute [17]. Our analysis revealed that similar to what has been observed for ACC metastatic to the liver, time to recurrence or progression after adrenalectomy and T stage of the primary tumor correlate significantly with survival of patients undergoing pulmonary metastasectomy. Several factors, including the number of metastatic lesions, chemotherapy prior to pulmonary resection, staged procedure, or pulmonary disease as the first site of recurrence, did not appear to influence survival. The presence of extra-adrenal disease at the time of primary adrenalectomy, and contralateral disease at the time of pulmonary metastasectomy tended to be associated with poor survival; however, our analysis is not conclusive enough to recommend against proceeding with pulmonary metastasectomy in patients with these potentially adverse factors who are otherwise good candidates for surgery. Adjuvant chemotherapy after adrenalectomy has been evaluated in several series, but neoadjuvant or adjuvant treatment for metastasectomy for ACC has not been well studied. Dickstein and colleagues [5] reported a benefit for adjuvant mitotane after primary adrenalectomy. Grubbs and Lee [6] observed no benefit if curative resection was performed. Crucitti and colleagues [9] also noted no benefit for adjuvant mitotane. Icard and colleagues [16] reported that mitotane was beneficial for patients undergoing palliative resection. In our study, adjuvant chemotherapy after adrenalectomy had no influence on survival of patients undergoing pulmonary metastasectomy; furthermore, neoadjuvant therapy prior to pulmonary metastasectomy did not improve survival, and may actually have been detrimental. Our observations that median OS and 5-year survivals GENERAL THORACIC

6 GENERAL THORACIC 1200 KEMP ET AL Ann Thorac Surg PULMONARY METASTASECTOMY FOR ACC 2011;92: from the date of first pulmonary resection for metastatic ACC are 40 months and 41%, respectively, are consistent with results reported by Crucitti and colleagues [9] for patients undergoing resection of recurrent or metastatic ACC in the Italian Registry. Our findings that RFS for patients rendered NED was 6 months, and PFS for patients with residual disease was 2 months, indicate that despite aggressive surgical debulking, pulmonary metastases quickly recur; however, patients with recurrent pulmonary metastases have reasonable long-term survivals and can tolerate multiple metastasectomy procedures. In the absence of a prospective randomized trial one cannot conclude that the metastasectomies prolong survival; nevertheless, our findings suggest this may be the case. Only 54% of these patients were rendered NED overall after the initial pulmonary resection; however, 88% were NED in the lungs. Given that most patients were NED in the lungs and only half were NED overall, we looked specifically at ipsilateral and contralateral disease progression to determine if a pattern to disease progression exists. The ipsilateral DFS and the PFS were 7 and 4 months, respectively, with approximately 25% in each group not having ipsilateral recurrences. These data suggest that one quarter of patients may achieve longterm disease control after initial complete pulmonary metastasectomy, which is a reasonable percentage given the fact that no systemic therapies can achieve these results. Contralateral disease progression was noted for patients who did not have an intervention in that hemithorax (n 15). For these patients, the DFS and PFS were 10 and 2 months, respectively. Progression of disease in the contralateral chest not undergoing resection suggests 2 points. First, patients with residual disease may have biologically more aggressive tumors given the shorter, although not statistically different, median survival. Second, patients who are NED after pulmonary metastasectomy can recur in a different site, which suggests the presence of disseminated microscopic disease. Despite small numbers, this study suggests that repeat pulmonary metastasectomies are feasible for select patients with thoracic recurrences after a pulmonary resection. Median OS after second pulmonary metastasectomy was 24 months and disease-free or progressionfree survivals after subsequent pulmonary resections were similar to those for the initial metastasectomy for ipsilateral (6 months versus 6 months), as well as contralateral (8 months versus 10 months) disease, respectively. Although this report represents the most thorough evaluation of patients undergoing pulmonary metastasectomy for ACC, our analysis suffers from limitations inherent in any retrospective review of nonstandardized treatment regimens. Clearly, referral of patients for treatment at our institution reflects a potential selection bias in favor of individuals with more favorable tumor biology and better performance status who might have longer disease-specific survivals irrespective of surgical intervention. Nevertheless, despite the limitations of the analysis, our experience indicates that pulmonary metastasectomy for ACC is potentially beneficial regardless of the number or bilaterality of lesions, or number of procedures required to treat evolving metastatic disease. Continued efforts should focus on identification of novel agents for treatment of metastatic ACC and validation of clinical and molecular variables that may guide future therapeutic interventions for patients with these neoplasms. References 1. Roman S. Adrenocortical carcinoma. Curr Opin Oncol 2006; 18: Vaughan, ED Jr. Diseases of the adrenal gland. Med Clin North Am 2004;88: Allolio B, Hahner S, Weismann D, Fassnacht M. Management of adrenocortical carcinoma. Clin Endocrinol (Oxf) 2004;60: Schulick RD, Brennan MF. Long-term survival after complete resection and repeat resection in patients with adrenocortical carcinoma. Ann Surg Oncol 1999;6: Dickstein G, Shechner C, Nativ O. Adjuvant mitotane in adrenocortical carcinoma. N Engl J Med 2007;357: Grubbs E, Lee JE. Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a revised TNM classification. Cancer 2009;115: Terzolo M, Angeli A, Fassnacht M, et al. Adjuvant mitotane treatment for adrenocortical carcinoma. N Engl J Med 2007; 356: Trainer PJ, Besser M. Cushing s syndrome. Therapy directed at the adrenal glands. Endocrinol Metab Clin North Am 1994;23: Crucitti F, Bellantone R, Ferrante A, Boscherini M, Crucitti P. The Italian Registry for Adrenal Cortical Carcinoma: analysis of a multiinstitutional series of 129 patients. The ACC Italian Registry Study Group. Surgery 1996;119: Favia G, Lumachi F, Carraro P, D Amico DF. Adrenocortical carcinoma. Our experience. Minerva Endocrinol 1995;20: Barrou Z, Billaud L, Guilhaume B, Bertagna X, Luton JP. Nodular adrenomegalies in congenital adrenal hyperplasia in adults. Implications. [Article in French] Presse Med 1990; 19: Hutter AM Jr, Kayhoe DE. Adrenal cortical carcinoma. Results of treatment with o,p DDD in 138 patients. Am J Med 1966;41: King DR, Lack EE. Adrenal cortical carcinoma: a clinical and pathologic study of 49 cases. Cancer 1979;44: Jensen JC, Pass HI, Sindelar WF, Norton JA. Recurrent or metastatic disease in select patients with adrenocortical carcinoma. Aggressive resection vs chemotherapy. Arch Surg 1991; 126: Fraker D. Adrenocortical carcinoma. In: Devita V, Lawrence T, Rosenberg S, eds. Cancer: principles and practice of oncology. Philadelphia, PA: Lippencott Williams & Wilkins; 2008: Icard P, Goudet P, Charpenay C, et al. Adrenocortical carcinomas: surgical trends and results of a 253-patient series from the French Association of Endocrine Surgeons study group. World J Surg 2001;25: Ripley R, Kemp C, Davis J, et al. Liver resection and ablation for metastatic adrenocortical carcinoma. Ann Surg Oncol 2011;18:

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