Surgery 000 (2018) 1-6
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Laparoscopic versus open adrenalectomy for localized (stage 1/2) adrenocortical carcinoma: Experience at a single, high-volume center
Kan Wu, MM+, Zhihong Liu, MD+, Jiayu Liang, MD, Yongquan Tang, MD, Zijun Zou, MD, Chuan Zhou, MM, Fuxun Zhang, MM, Yiping Lu, MD*
Department of Urology, Institute of Urology, West China Hospital, Sichuan University, China
| ARTICLE INFO | ABSTRACT |
|---|---|
| Article history: Accepted 23 July 2018 Available online xxx | Background: Open adrenalectomy is considered a standard operative approach for adrenocortical carci- noma, and laparoscopic adrenalectomy remains controversial. We analyzed our outcomes of laparoscopic adrenalectomy and open adrenalectomy for localized (stage 1/2) adrenocortical carcinoma in our hospital. Methods: This study retrospectively reviewed all patients with stage 1/2 adrenocortical carcinoma and a tumor size < 10 cm who underwent radical resection in our hospital between 2009 and 2017. These patients were divided into laparoscopic adrenalectomy and open adrenalectomy groups. Demographics, operative data, and follow-up outcomes were collected. The 5-year overall survival and recurrence-free survival were calculated with the Kaplan-Meier method and compared between laparoscopic adrenalec- tomy and open adrenalectomy group. Results: A total of 23 patients operated by an open adrenalectomy and 21 patients operated with a la- paroscopic adrenalectomy were included. Baseline patient characteristics (age, sex, tumor size, hormonal secretion) were similar between 2 groups. The mean postoperative stay was less in the laparoscopic adrenalectomy group (P =. 003). The mean follow-up time was similar for the two groups (33 ± 24 vs 35 ± 25 months; P=NS). The local and peritoneal recurrence rates were 42% for laparoscopic adrenalec- tomy and 22% for open adrenalectomy (P =. 035). Time to local and peritoneal recurrence was less in the laparoscopic adrenalectomy than in the open adrenalectomy (P =. 048). The 5-year overall survival and recurrence-free survival for open adrenalectomy versus laparoscopic adrenalectomy were 43% vs 47% (P =. 635) and 36% vs 39% (P =. 802), respectively. Conclusion: We believe that open adrenalectomy should still be considered the standard operative man- agement of adrenocortical carcinoma. Laparoscopic adrenalectomy may not provide patients with local- ized adrenocortical carcinoma with an equivalent oncologic outcome based on site and timing of initial tumor recurrence. @ 2018 Elsevier Inc. All rights reserved. |
Introduction
Adrenocortical carcinoma (ACC) is a rare but deadly endocrine malignancy, with an annual incidence of approximately two per million population. Its prognosis was often poor because of the
high rate of recurrence.1,2 Despite complete initial resection, recur- rence occurs in up to two-thirds of patients. Patients with early- stage disease who undergo a complete resection have a 5-year survival of about 40%.3 Unfortunately, adjuvant therapies have not been successful, radiation and chemotherapy are largely ineffective, and the role of mitotane is unproven. Therefore, operative resec- tion by an open approach (OA) has traditionally been the mainstay of treatment, allowing for a margin-free complete resection.
Initially described in 1992, laparoscopic adrenalectomy (LA) has become the standard treatment for benign adrenal masses, both functioning and nonfunctioning. LA has been shown to have less pain, less perioperative morbidity, and a shorter hospital stay com- pared with an OA.4 More recently, the role of robot-assisted la- paroscopy has been suggested for adrenal surgery.5 The increasing
* Supported by the Science and Technology Foundation of Sichuan Province (2017SZ0123 to Zhihong Liu) and 1.3.5 project for disciplines of excellence, West China Hospital, Sichuan University.
* Corresponding author: Yiping Lu, Professor of Urology, Department of Urol- ogy, Institute of Urology, West China Hospital Sichuan University, 37 Guoxue Lane chengdu, Sichuan 610041 China.
E-mail address: yipinglu@163.com (Y. Lu).
1 Kan Wu and Zhihong Liu contributed equally to this work and should be re- garded as first co-authous.
https://doi.org/10.1016/j.surg.2018.07.026
K. Wu et al./Surgery 000 (2018) 1-6
experience with LA and excellent results of this approach have led some authors to also propose LA for potentially malignant adrenal tumors. Favorable oncologic outcomes after LA for ACC have been suggested in several small studies. In experienced referral centers, LA is even now used increasingly for large adrenal lesions and adrenal metastases.6,7 However, in cases of ACC, very few stud- ies have provided a comparative analysis of the outcomes between OA versus LA for this specific entity, and previous findings from these studies have been conflicting. Some reports have suggested that the LA should be avoided in cases where ACC is suspected be- cause of an increased risk of positive surgical margins or tumor spill, peritoneal carcinomatosis, and earlier recurrence.8 Recently, a meta-analysis revealed that there were no differences in the over- all recurrence rate and time to recurrence between LA and OA, whereas development of peritoneal carcinomatosis was greater for LA.9 In contrast, a single-institution study of operative treatment of 34 patients with stage 1-2 ACC suggested that LA can achieve similar results in terms of recurrence rate as OA for patients with potentially malignant adrenal tumors with a size < 10 cm and no evidence of extra-adrenal extension.10
The question that requires answering for surgeons is how to choose an appropriate operative approach for ACC according to tumor size and preoperative characteristics on imaging. Conse- quently, the purpose of our study was to report a single, high- volume center experience of LA versus OA in the treatment of pa- tients with localized (stage 1/2) ACC.
Methods
Approval from our institutional review board was obtained for the study. We retrospectively reviewed all patients with ACC at West China Hospital, Sichuan University (Sichuan, China) between January 2009 and September 2017. All cases were confirmed by pathologic review. Among this cohort of patients, we then selected all in whom LA could be considered, based on the current crite- ria (lesion < 10 cm, with no radiologic sign of local invasion).11,12 Therefore, we initially excluded patients with extra-adrenal exten- sion corresponding to stages 3 and 4, according to the classification of the European Network for the Study of Adrenal Tumors (ENSAT), and those with a lesion > 0 cm on preoperative computed tomog- raphy (CT). All remaining patients (ie, those with ENSAT stage 1/2 tumors < 10cm) undergoing LA and OA in our hospital were in- cluded in the study.
In the retrospective comparative study, demographics, primary diagnosis (including functional status), imaging data, operative de- tails, hospital stay, pathology, postoperative stage (based on patho- logic assessment), adjuvant therapy, and follow-up results were collected and compared between ACC patients who underwent LA and OA. The study endpoint was to compare the oncologic effec- tiveness of the LA and OA as evaluated by overall survival (OS) and recurrence-free survival (RFS). Recurrent disease was diagnosed on the basis of clinical, radiographic, and laboratory evidence. Tumors that were located in the operative site were regarded as local re- currence; peritoneal carcinomatosis was diagnosed on postopera- tive CT when there was obvious abnormal parietal peritoneal thick- ening, parietal peritoneal enhancement, and enhancing nodules. All other unexplained tumor-like lesions were considered to be distant metastases. Pathologic confirmation was not deemed necessary for the diagnosis of recurrent disease with these criteria. OS was cal- culated from the date of operation to death or to the last follow- up date. RFS was calculated from the date of operation to the date of diagnosis of tumor recurrence or to the date of last follow-up without recurrence.
Results are described as mean ± SD (standard deviation) or me- dian (range). Comparisons were performed with Fisher exact tests, x2 analysis, and the Mann-Whitney U test as appropriate. Survival ☒
curves were calculated according to the Kaplan-Meier method, and comparisons between groups of patients were made using a log-rank test. We used SPSS software v 18.0 (IBM, Armonk, NY) to perform the statistical analysis. A difference was considered statis- tically significant when P < . 05. We acknowledge that these sta- tistical estimates are somewhat limited by the number of available patients.
Results
Figure 1 illustrates the selection of patients who were included in the present study. Among a total of 65 consecutive patients who underwent adrenalectomy for ACC, 16 had ENSAT stage 3 or 4 lesions and were excluded from this study. All these latter pa- tients were submitted to OA, except for 2 patients presenting with adrenal incidentaloma who underwent LA and those found to have microscopic invasion of periadrenal fat, based on final pathology (stage III after operation), were excluded from the study. Among the 49 remaining patients with ENSAT stage I/II, 5 had an adrenal tumor larger than 10 cm and were therefore excluded and were treated with OA. The 44 remaining patients had ENSAT stage 1 or 2 adrenal lesion < 10 cm and were included in the study, 23 of whom underwent OA and 21 of whom underwent LA.
The characteristics of the study population are summarized in the Table 1. LA was performed using the retroperitoneal approach in 12 cases and the lateral transabdominal approach in 11 cases. One patient was converted to an open procedure because of tu- mor rupture. This patient was recurrence-free 4 months later. The two groups were well-matched for age, sex, secreting tumor, tumor size, and stage (P=NS; Table 1).
Regional lymph node dissection was performed in 3 patients in the OA group. Adjunctive procedures were performed in 3 pa- tients in the OA group, including 2 nephrectomies, and liver re- section, splenectomy, and distal pancreatectomy in 1 patient each. The mean operative time was similar in the OA group and the LA groups (117 ± 56 versus 125 ± 35, respectively; P =. 362; Table 1).
Postoperative complications occurred in 2 of the 23 patients in the OA group and 1 of the 21 patients in the LA group (P =. 99). The mean postoperative stay was significantly less after LA than after OA (6 ± 2 versus 9 ± 4 days, P =. 002).
The presence of microscopic capsular invasion was present in 26% (6 of 23) of OA patients and 33% (7 of 21) of LA patients (P =. 599). The Weiss score and Ki-67 were similar between the 2 groups (P=NS; Table 1).
The mean duration of follow-up was similar in both groups: 33 ± 24 months (range, 3-104) in the OA and 35 ± 25 (range, 3-99) in the LA (P =. 724; Table 1). Adjuvant therapy was given in 4 of 23 patients in the OA group and 2 of 21 patients in the LA group (P =. 749).
Overall, recurrent disease (local, peritoneal, and distant) oc- curred in 52% of OA cases and 52% of LA cases (P =. 989). The mean time to recurrence was 22 ± 24 months in the OA group and 25 ± 22 in the LA group (P =. 564). The rate of local recurrence was 22% (5 of 23) in the OA group and 43% (9 of 21) and in the LA group (P =. 13). Distant metastases occurred in 30% of the OA cases and 24% of the LA cases (P =. 622). The rate of peritoneal carcinomato- sis was 1 of 23 in the OA group and 5 of 21 and in the LA group (P =. 15).
At the initial diagnosis of recurrence, a combined pattern of re- current disease (local and peritoneal recurrence) was greater in the LA group than in the OA group (42% [11 of 21] versus 22% [5 of 23], P =. 035). Mean time to recurrence in the local and peritoneum was less in the LA group (40 ± 8 months vs 79 ± 9; P =. 048; Fig 2).
At the most recent follow-up, 16 (36 %) patients had died, including 9 (39 %) OA patients and 7 (33 %) LA patients (P =. 690). The median RFS was 24 months in the both groups (P =. 802,
Please cite this article as: K. Wu et al., Laparoscopic versus open adrenalectomy for localized (stage 1/2) adrenocortical carcinoma: Experience at a single, high-volume center, Surgery (2018), https://doi.org/10.1016/j.surg.2018.07.026
ARTICLE IN PRESS
Overall surviaval
Adrenocortical carcinoma 65
100
80-
LA
Overall survival (%)
OA
Stage I/II 49
Stage III/IV 16
60.
40.
Stage I/II ≥ 10 cm 5
Stage I/II < 10 cm 44
20-
P=0.372
0
0
24
48
72
96
120
Open 23
Laparoscopic 21
Months
| Variable | All patients n=44 | OA group n=23 | LA group n=21 | P value |
|---|---|---|---|---|
| Baseline characteristic | ||||
| Age, yr, mean ± SD (range) | 45.2 ± 15.2 (2-74) | 45.6 ± 14.5 (5-71) | 44.9 ± 16.2 (2-74) | 0.805 |
| Female gender, n (%) | 27 (61.4) | 13 (56.5) | 14 (66.7) | 0.490 |
| Right side, n (%) | 15 (34.1) | 6 (26.1) | 9 (42.9) | 0.241 |
| Secreting tumor, n (%) | 20 (45.5) | 9 (39.1) | 11 (52.4) | 0.378 |
| Tumor size (mm) | 63.6 ± 20.7 (20-98) | 68.7 ± 20.9 (20-98) | 58.0 ± 19.4 (26-88) | 0.075 |
| Mean ± SD (range) | ||||
| Tumor stage, n (%) | ||||
| I | 9 (20.5) | 3 (13.0) | 6 (28.6) | 0.367 |
| II | 35 (79.5) | 20 (87.0) | 15 (71.4) | |
| Surgical outcomes | ||||
| Lymph node dissection | 3 | 3 | 0 | |
| Adjunctive procedures, n (%) | 3 | 3 | 0 | |
| Conversion to open, n (%) | - | NA | 1 (4.8) | |
| Operation time (min) | 121 ± 47 (40-260) | 117 ± 56 (40-260) | 125 ± 35 (40-200) | 0.362 |
| Mean ± SD (range) | ||||
| Postoperative complication | 3 | 2 | 1 | 1.000 |
| Postoperative stay (d) | 7.5 ± 3.4 (2-22) | 8.6 ± 4.0 (2-22) | 6.3 ± 2.0 (3-12) | 0.002 |
| Mean ± SD (range) | ||||
| Pathology findings | ||||
| Capsular invasion, n (%) | 13 (29.5) | 6 (26.1) | 7 (33.3) | 0.599 |
| Weiss score, median (range) | 5.0 (3.0-7.0) | 5.0 (4.0-7.0) | 4.0 (3.0-7.0) | 0.084 |
| Ki-67, median (range) | 8.0 (2.0-45.0) | 8.0 (4.0-45.0) | 8.0 (2.0-42.0) | 0.848 |
| Follow-up outcomes | ||||
| Adjuvant therapy, n (%) | 6 (13.6) | 4 (17.4) | 2 (9.5) | 0.749 |
| Follow-up (months) | 34 ± 25 (3-104) | 33 ± 24 (3-104) | 35 ± 25 (3-99) | 0.724 |
| Mean ± SD (range) | ||||
| Recurrence, any site n (%) | 23 (52.3) | 12 (52.2) | 11 (52.4) | 0.989 |
| Local | 14 (31.8) | 5 (21.7) | 9 (42.9) | 0.133 |
| Peritoneal cavity | 6 (13.6) | 1 (4.3) | 5 (23.8) | 0.150 |
| Distant | 12 (27.3) | 7 (30.4) | 5 (23.8) | 0.622 |
| Time to recurrence | 23 ± 23 (3-104) | 22 ± 24 (3-104) | 25 ± 22 (3-79) | 0.564 |
| Mean ± SD (range) | ||||
| Cancer specific deaths, n (%) | 16 (36.4) | 9 (39.1) | 7 (33.3) | 0.690 |
Fig 3). The median OS was 42 and 63 months for OA and LA patients, respectively (P =. 635, Fig 4). The 5-year RFSs and OSs for OA versus LA were 36 vs 39 % (P =. 802) and 43 vs 47 % (P =. 635), respectively (Figs 3 and 4).
Discussion
In the present study, we reviewed a nearly 10-year experience with the surgical treatment of localized (stage 1/2) ACC at our in- stitution. We identified association of LA with faster postoperative recovery. In terms of RFS and OS, we were unable to identify any statistically significant differences based on surgical technique. In addition, we evaluated the efficacy of the 2 surgical techniques, separating local and peritoneal cavity recurrence, which are more
likely relevant to the resection technique itself, from more distant metastasis that are likely influenced by tumor biology. It is indi- cated that patients who undergo LA experience higher rates of lo- cal and peritoneal cavity recurrence and develop recurrence in the local and peritoneum significantly earlier than patients who un- dergo OA. The results imply some type of inherent difference in the techniques, and LA increases the risk of local and peritoneal cavity recurrences. As such, our study suggests that patients with known or suspected ACC should be strongly considered for OA, and LA may not be safely proposed to patients with potentially malig- nant adrenal tumors with a size <10 cm and no evidence of extra- adrenal invasion.
With the widespread diffusion of LA, a greater percentage of patients with adrenal incidentaloma were referred to adrenalec-
ARTICLE IN PRESS
Recurrence-free survival
Time to local and peritoneal recurrence
100
100
-
LA
- LA
Recurrence-free survival (%)
80-
OA
Cumulative recyurrence(%)
80
OA
60-
60.
40-
40.
P = 0.048
20-
P=0.871
20-
0
0
0
24
48
72
96
120
0
24
48
72
96
120
Months
Months
Recurrence-free survival
Time to tumor bed or peritoneal recurrence
100
100
LA
Recurrence-free survival (%)
LA
80-
- OA
Cumulative recyurrence(%)
80-
OA
60.
60-
40.
40
20
P = 0.802
20
P=0.043
0
0
0
24
48
72
96
120
0
24
48
72
96
120
Months
Months
Overall surviaval
100
-
LA
-
OA
80
Overall survival (%)
60.
40-
P = 0.635
20-
0
0
24
48
72
96
120
Months
tomy. Moreover, in the absence of radiologic evidence of the inva- sion of surrounding tissues, lymph node involvement, intravenous thrombus, or distant metastases, may be difficult to predict malig- nancy in adrenal incidentaloma. Indeed, about 10% of the resected adrenal incidentaloma have a pathologic diagnosis of ACC.13,14 As a consequence, LA emerged as the treatment of choice for most
adrenal tumors. However, surgeons must carefully take into ac- count tumor size and preoperative imaging characteristics when making an appropriate choice regarding type of surgery. Recently published guidelines from the European Society of Endocrine Sur- geons suggest that laparoscopic resection is acceptable if imaging appears to suggest a stage 1 or 2 tumor ≤10 cm.11,12
Several authors have previously suggested favorable oncologic outcomes of LA for ACC.10,15,16 Donatini et al10 reviewed a single- institution experience with surgical treatment of 34 ACC cases (stage 1-2) and found no differences in RFS and OS. This find- ing resembled results reported by Brix et al15 based on data from a German ACC registry; 152 patients with ENSAT stage 1-3 ACC neoplasms measuring < 10 cm were included, 35 underwent LA, and 117 underwent OA. The recurrence rate was 77% for the LA groups and 69% for the OA groups. No significant differences were found in OS or RFS. Similarly, Mir et al16 reported that a signif- icant reduction was not observed in recurrence and death rate between patients undergoing OA and LA after adjusting for clini- cal stage (hazard ratio [HR] 0.4; 95% confidence interval [CI] 0.2- 1.2; P =. 099; HR 0.5; 95% CI 0.2-1.2; P =. 122; respectively). Like- wise, the 2 largest studies comparing LA with OA are based on the multi-institutional analysis, namely the one reported by the Ger- man Adrenocortical Carcinoma Registry Group and the one based on Italian multi-institutional survey.17,18 The German ACC Registry Group11 analysis reported that the results of its multicenter OA versus LA series for localized ACC neoplasms measuring <10 cm
Please cite this article as: K. Wu et al., Laparoscopic versus open adrenalectomy for localized (stage 1/2) adrenocortical carcinoma: Experience at a single, high-volume center, Surgery (2018), https://doi.org/10.1016/j.surg.2018.07.026
found that median disease-free survival after LA was 24 months. Lombardi et al18 reviewed the Italian multi-institutional survey with surgical treatment of 156 patients with ACC (stage 1-2) who underwent R0 resection. Because no differences were found in on- cologic outcomes, they concluded that LA is acceptable for local- ized ACC if proper patient selection is embraced and principles of surgical oncology are respected. In a word, the authors did not find any significant difference in terms of RFS or OS. From our results, we were also unable to identify any statistically significant differ- ences based on surgical technique. However, we found that LA may increase the risk of local and peritoneal cavity recurrences for pa- tients with localized (stage 1/2) ACC.
In general, the majority of previous reports comparing laparo- scopic versus open resection for ACC have limitations. First and foremost, most of them report on a limited number of cases, espe- cially for the laparoscopic cohorts. Moreover, despite being of good quality, all of these studies are retrospective case-control series, implying a patient selection bias. Nevertheless, patients undergo- ing OA had larger mean size of tumors and advanced disease.
Moreover, one cannot assume that 2 surgical approaches are equivalent based solely on similar overall survival because tumor biology plays a significant role in distant metastases and survival. Studies should differentiate between local and peritoneal cavity re- currence most likely related to technical issues. Distant metastasis is more likely affected by tumor biology. Indeed, the use of endo- scopic instruments to manipulate the adrenal neoplasms implies the theoretic risk of inadvertent tumor capsule fracture and tu- mor cell dispersion in the peritoneal cavity, with consequent lo- cal and peritoneal carcinomatosis. This concern is particularly true for large adrenal neoplasms and in the case of difficult dissection because of tumor adhesion with adjacent structures.19 From our results, we could not find any differences between LA and OA in most relevant oncologic outcomes, including the overall recurrence rate, time to recurrence, and cancer-specific mortality. However, there was higher risk of local and peritoneal carcinomatosis and mean time to recurrence in the local and peritoneum was signif- icantly shorter after LA. The finding is in line with the study by Leboulleux et al,20 who found that the only risk factor of peritoneal carcinomatosis after surgery was the surgical approach (P =. 016), and data reported by the MD Anderson group (Houston, TX),21 who found a high risk of peritoneal carcinomatosis after LA (83% [5 of 6 cases]) versus OA (8% [11 of 133 cases]). Similarly, Miller et al22 presented a retrospective review of 46 LA and found that the time of visible tumor bed or peritoneal recurrence in stage 2 patients was shorter in LA patients (P =. 002). Recently, a systematic re- view and meta-analysis also found the incidence of peritoneal car- cinomatosis was higher after LA than OA (P =. 001).9 These find- ings suggest that OA is superior to LA in the management of ACC. Therefore, to avoid jeopardizing the oncologic outcome, future studies should consider the outcome based on what the suspected preoperative stage was and differentiate between recurrences most likely related to surgical technique rather than those more likely affected by tumor biology.22
Conversion to the open approach is recommended in cases where signs of local invasion are found or the dissection is difficult and implies the risk of tumor capsule rupture, whereas a strict pa- tient selection likely contributed to limiting the risk of tumor cap- sule rupture. Donatini et al10 found no conversion to laparotomy in 13 consecutive patients with localized ACC neoplasms measur- ing <10 cm. We also just found 1 conversion to laparotomy in the LA group (the maximum tumor size is 8.8 cm). Therefore, conver- sion should not be considered a defeat for the surgeon but rather a different way to safely accomplish the surgical procedure. Nev- ertheless, surgical technique must be optimized in anticipation of a time when additional, more efficacious therapies are available. It is an opportunity and responsibility for the surgeon to limit local
and peritoneal recurrence because distant metastases likely cannot be greatly influenced by type of surgery.22
Recent reports indicate that locoregional lymph node dissection (LND) may improve oncologic outcome in patients with localized ACC who may benefit from both better staging with standardized LND and a potential micrometastatic LND.23 However, there is con- troversy regarding the extent and time for LND in ACC. In our se- ries, LND was performed in selected cases only and, as a result, we could not draw any conclusions on this issue.
The present study is a single-institution retrospective analysis and it has limitations. First, selection bias cannot be eliminated. Indeed, in clinical practice, smaller tumors are selected for LA and locally infiltrating and metastatic tumors are selected mandatorily for OA. To minimize this risk, we chose to include only patients with pathologically proven localized (stage 1/2) ACC. It is notewor- thy that patient and tumor characteristics were strictly similar in both study groups (Table 1), which may have somewhat reduced the number of our cohort, but considerably reduced the possible biases. Second, this study examines the role of surgical technique in disease outcome by evaluating initial local and peritoneal cavity recurrences rather than using all sites of recurrence noted at any time during the disease course because local and peritoneal cavity recurrence is most likely relevant to inadequate surgical manipu- lation, but distant metastasis is not greatly influenced by surgical types. Third, surgical margin status (R0/R1 margin) for ACC is not assessed by pathology specimens at our institution; it would be associated with RFS and OS.24 But we evaluated the presence of microscopic capsular invasion and excluded patients who under- went macroscopically incomplete (R2) resections in an attempt to debulk the tumor. Last, the follow-up is relatively short and the sample size is relatively small; additional series would be of great value. A wide prospective randomized trial on this topic is not likely to be performed because the malignancy is rare and most of diagnoses in localized neoplasms are pathologic.
In conclusion, OA should still be considered the standard sur- gical management of ACC. LA may not provide patients with an equivalent oncologic outcome in terms of site and timing of initial tumor recurrence, even if the tumor size is <10 cm and there is no evidence of extra-adrenal invasion.
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Please cite this article as: K. Wu et al., Laparoscopic versus open adrenalectomy for localized (stage 1/2) adrenocortical carcinoma: Experience at a single, high-volume center, Surgery (2018), https://doi.org/10.1016/j.surg.2018.07.026