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Association for Academic Surgery
Minimally Invasive Surgery for Resectable Adrenocortical Carcinoma: A Nationwide Analysis
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Aaron M. Delman, MD, MS,a,b Kevin M. Turner, MD,a,b Azante Griffith, BS,” Emily Schepers, MD,a,b Allison M. Ammann, MD,a,b and Tammy M. Holm, MD, PhD, FACSa,b,*
a Department of Surgery, University of Cincinnati, Cincinnati, Ohio
b Cincinnati Research on Outcomes and Safety in Surgery (CROSS) Research Group, University of Cincinnati, Cincinnati, Ohio
ARTICLE INFO
Article history: Received 29 December 2021 Received in revised form 4 March 2022 Accepted 23 April 2022 Available online 30 June 2022
Keywords:
Adrenal tumors Adrenocortical carcinoma Guidelines adrenocortical carcinoma Laparoscopic resection Minimally invasive surgery Robotic resection
ABSTRACT
Introduction: The utilization of minimally invasive surgery (MIS) for adrenocortical carci- noma (ACC) remains controversial due to concerns regarding the quality of surgical resection and subsequent oncologic risks. Current guidelines recommend open resections for all cases of suspected ACC independent of size; however, there has been increased adoption of MIS for ACC over time. We sought to determine whether the rise in the utili- zation of MIS is associated with worse survival outcomes for ACC.
Methods: The National Cancer Database was queried for patients with ACC who underwent surgical resection between 2010 and 2017. Patient selection, oncologic outcomes, and overall survival were compared among patients who received an MIS approach (laparo- scopic or robotic) versus an open approach.
Results: A total of 1483 patients underwent ACC resection with 982 (66.2%) patients un- dergoing an open approach and 501 (33.8%) receiving an MIS operation. The overall utili- zation of MIS for ACC increased significantly after 2013 (37.7% versus 29.5%, P < 0.01). There was no difference in overall survival between MIS and open resections on univariable (log- rank P = 0.12) analysis. On multivariable analysis, survival was improved in MIS patients versus open resection (Hazard ratio: 0.83, 95% CI: [0.70-0.99]). Notably, survival remained comparable among patients who underwent resection for large ACCs (6-10 cm, log-rank P = 0.66) and giant ACCs (>10 cm, log-rank P = 0.24), irrespective of operative approach. Conclusions: Our findings suggest that in appropriately selected patients with ACC, MIS can be performed safely without a significant decrease in overall survival, independent of size. We recommend consideration of a minimally-invasive approach for adrenal masses despite size >6 cm.
@ 2022 Elsevier Inc. All rights reserved.
* Corresponding author. Assistant Professor of Surgery, Department of Surgical Oncology, The University of Cincinnati, 231 Albert Sabin Way, MSB 1466, Cincinnati, OH 45219. Tel .: +1 513 558 4748; fax: +1 513 584 0459. E-mail address: tammy.holm@uc.edu (T.M. Holm).
Introduction
Adrenocortical carcinoma (ACC) is an aggressive endocrine malignancy with a somber five-year survival rate of 32-50% following resection.1-3 Poor survival following resection of ACC is largely attributed to its late clinical presentation and high rates of locally advanced or metastatic disease at the time of diagnosis.4,5 Radiation and chemotherapy are largely ineffec- tive in the management of ACC, therefore, complete surgical resection with negative margins remains the primary deter- minant of survival.3,6 A minimally invasive (MIS) approach to benign adrenal lesions is preferred but the potential risks of tumor spillage, positive margins, and increased recurrence with MIS resection for ACC have tempered enthusiasm for the MIS approach.7,8 Given the higher risk of malignancy in adrenal tumors relative to size, current guidelines recommend an open approach for all lesions suspicious for ACC >4 cm.9,10
The evidence regarding the oncologic safety of an MIS approach for ACC remains controversial.11,12 Early retrospec- tive case-series have described an increased risk of local and peritoneal recurrence, decreased disease-free survival, and decreased overall survival with an MIS approach.8,13,14 How- ever, other similar retrospective investigations have demon- strated benefits to an MIS approach for ACC with improved length of stay and decreased blood loss in conjunction with similar rates of tumor rupture, margin positivity, and both overall and disease free survival.3,15,16 Conflicting data regarding the relative risks and benefits of an MIS versus open approach for ACC is highlighted by the variation in guideline recommendations with respect to surgical approach. The National Comprehensive Cancer Network (NCCN) states there may be an increased risk of local recurrence and peritoneal spread with an MIS approach. They suggest open resection for suspected, resectable ACC with the caveat that an MIS approach may be considered based on “tumor size and degree of concern regarding potential malignancy, and local surgical expertise.”9 The American Association of Endocrine Surgeons /American Association of Clinical Endocrinologists (AACE) guidelines recommend open resection for all cases of ACC, irrespective of tumor size.10 While guidelines continue to suggest that an open approach is preferred for known or suspected ACC, it is evident adrenal surgeons have become increasingly comfortable with the MIS approach and utiliza- tion in the setting of ACC is rising.17 We aimed to determine whether a MIS approach associates with decreased survival in a nationwide cohort of ACC patients.
Materials and Methods
Data source & study population
The American College of Surgeons and American Cancer So- ciety clinical oncology National Cancer Database (NCDB) participant user file (PUF) for endocrine malignancies was queried to identify patients with ACC. The NCDB includes over 1500 Commission on Cancer accredited facilities and repre- sents more than 70% of newly diagnosed cancer cases nationwide.18 Figure 1 is a consort figure describing how the
final cohort of patients was isolated from the NCDB. Briefly, the international classification of diseases for oncology (ICD-O-3) topography code for the site of malignancy was used to isolate only adrenal tumors (C740/C741/C749) between the years of 2010-2017. Patients who did not undergo surgery were excluded. Only patients with ACC as their histology code in the ICD-O-3 (8370) were included in the final analysis. Patients were classified by the initial operative approach, in an intention-to-treat fashion: robotic and laparoscopic ap- proaches were classified as minimally invasive (MIS), and these were compared to patients who underwent standard open resection. Procedures which were initiated MIS and subsequently converted to open were included in the MIS cohort utilizing an intention to treat approach. Clinical staging was determined by the American Joint Committee on Cancer (AJCC) seventh edition.19 This investigation was reviewed by the University of Cincinnati Institutional Review Board and determined to be non-human subjects research (IRB ID: 2021-1158).
Statistical analysis
Baseline patient demographics and clinical characteristics were compared between patients who underwent MIS versus open resection of ACC. Descriptive statistics were described using mean ± standard deviation for normal distributions and median [interquartile range] for non-parametric distributions.
Endocrine PUF File (2004-2017) n=134,998
Excluded: Pituitary (n=111,421) Thymus (n=10,928) Pineal (n=2,131) Craniopharyngeal (n=2,837) Parathyroid (n=1,051) Other (n=452)
Adrenal Tumors (2004-2017) (n=6,178)
Excluded: Prior to 2010 (n=2,430) No surgical procedure (n=295)
No operative approach coded (n=1,353) Non ACC on histology (n=617)
ACC on final histology (n=1,483)
Comparisons of normally distributed variables were completed with two-sample t-tests, while non-parametric distributions were compared with the Wilcoxon rank-sum test. Categorical variables were assessed with the chi-square analysis. Differences were considered statistically significant for P-values <0.05. Patient survival was assessed with time-to- event Kaplan-Meier estimates based on a patients most recent follow-up. Multivariable Cox-proportional hazards models were constructed that included the following preop- erative characteristics: patient age at diagnosis, Charlson- Deyo Comorbidity Index, and tumor size. Models were assessed by Akaike information criterion (AICc) and scaled Schoenfeld residuals. To better assess whether tumor size plays a role in survival, a subset analysis was performed on patients with large ACCs (6 cm-10 cm) and giant ACCs (≥10 cm) and survival was compared between MIS and open resection. All statistical analysis was conducted in JMP PRO version 16.0 (SAS Institute Inc, Cary, NC, 1989-2019) and SAS version 9.4 (SAS Institute Inc, Cary, NC, 1989-2019).
Results
Study population
Between 2010 and 2017, there were 1483 patients who un- derwent resection for ACC with an identified surgical
Operative approach to adrenocortical carcinoma by year
150
Number of resections
100
50
Open
Minimally Invasive
0
2010
2011
2012
2013
2014
2015
2016
2017
Year
approach in the NCDB. 501 patients (33.8%) underwent MIS resection and 982 (66.2%) underwent open resection. In the entire cohort, the median age at diagnosis was 56 [IQR: 44-67] and the cohort was 60.9% female (n = 903). Most
| Table 1 - Patient demographics and clinical characteristics stratified by operative approach. | |||
|---|---|---|---|
| Characteristic | MIS (n = 501, 33.8%) | Open (n = 982, 66.2%) | P-value |
| Age, y, median [IQR] | 59 [48-68] | 55 [43-73] | <0.01 |
| Gender, f, n (%) | 312 (62.3%) | 591 (60.2%) | 0.44 |
| Race, n (%) | 0.47 | ||
| White | 437 (87.2%) | 843 (85.9%) | |
| Black | 45 (9.0%) | 89 (9.1%) | |
| Asian | 8 (1.6%) | 29 (3.0%) | |
| Other | 11 (2.2%) | 21 (2.1%) | |
| Hispanic ethnicity, y, n (%) | 28 (5.6%) | 63 (6.4%) | 0.53 |
| Primary insurance payer, n (%) | 0.04 | ||
| Private | 253 (51.1%) | 527 (55.5%) | |
| Government | 225 (45.5%) | 373 (39.3%) | |
| Not insured | 17 (3.4%) | 50 (5.3%) | |
| Charlson-Deyo Comorbidity score, mean ± SD | 0.47 ± 0.76 | 0.33 ± 0.64 | <0.01 |
| Facility Type, n (%) | <0.01 | ||
| Academic/research program | 221 (50.1%) | 496 (63.3%) | |
| Community cancer program | 15 (3.4%) | 23 (2.9%) | |
| Comprehensive community cancer program | 144 (32.7%) | 183 (23.3%) | |
| Integrated network cancer program | 61 (13.8%) | 61 (13.8%) | |
| Median income quartile, n (%) | <0.01 | ||
| Q1: < $38,000 | 75 (17.1%) | 133 (14.9%) | |
| Q2: $38,000-$47,999 | 83 (18.9%) | 222 (24.9%) | |
| Q3: $48,000-$62,999 | 110 (25.1%) | 256 (28.7%) | |
| Q4: >$63,000 | 171 (38.9%) | 280 (31.4%) | |
| MIS = minimally invasive surgery. | |||
A Overall survival of patients with adrenocortical carcinoma
100
- MIS
Percent Survival
- Open
50
log-rank p = 0.12
0
0
20
40
60
Months
| # at risk: | ||||
| MIS: | 432 | 285 | 159 | 78 |
| Open: | 858 | 555 | 332 | 172 |
B Overall survival of large (6-10cm) adrenocortical carcinoma
Probability of Survival
100
- MIS
- Open
50
log-rank p = 0.66
0
0
20
40
60
Months
# at risk:
MIS:
170
111
58
31
Open:
206
131
72
39
C Overall survival of giant (>10cm) adrenocortical carcinoma
100
Probability of Survival
- MIS
- Open
50
log-rank p = 0.24
0
0
20
40
60
Months
# at risk:
MIS:
122
69
33
13
Open:
540
351
213
109
patients identified as White (86.3%, n = 1280), followed by Black (9.0%, n = 134), Asian (2.5%, n = 37), and Other (2.2%, n = 32). 451 patients (33.9%) had a median annual household income in the highest quartile nationally (>$63,000). Most patients were privately insured (n = 780, 54.0%), followed by government insurance (n = 598, 41.4%). Only 67 (4.6%) pa- tients were uninsured. At the time of resection, 135 (12.2%) patients had clinical stage I disease, 496 (44.9%) clinical stage II, 166 (15.0%) clinical stage III, and 307 (27.8%) clinical stage IV disease. The median tumor size was 105 mm (70 mm-150 mm) after resection.
Utilization of minimally invasive surgery
Utilization of minimally invasive approaches for ACC increased significantly after 2013 (37.7% versus 29.5%, P < 0.01). Figure 2 displays the number of MIS and open resections for ACC by year. Patients who underwent an MIS resection were more likely to be older (59 versus 55, P < 0.01), have a higher Charlson-Deyo Comorbidity score (0.47 versus 0.33, P < 0.01), and were less likely to be uninsured (3.4% versus 5.3%, P = 0.04) (Table 1). Patients treated at an academic/research facility were more likely to receive an open resection (63.3% versus
Multivariable proportional hazards survival functions
1.0
Cumulative survival
0.5
Surgical Approach
MIS
0.0
Open
HR: 0.83, 95% CI: [0.70-0.99]
0
50
100
Time (months)
50.1%, P < 0.01). The MIS cohort had smaller tumors (75 mm versus 120 mm, P < 0.01) and were more likely to have clinical stage I disease (23.5% versus 6.9%, P < 0.01). Among the 501 patients who began the operation MIS, 79 (15.8%) were con- verted to an open approach. These patients are included in the MIS cohort for the entire analysis. Supplementary Table 1 details the clinical characteristics and oncologic outcomes between the cohorts by operative outcome.
Survival outcomes
There was no survival difference between patients who underwent MIS resection for ACC compared to those who underwent open resection (log-rank P = 0.12, Fig. 3A). Both 30-day mortality (1.2% versus 2.6%, P = 0.10) and 90-day mor- tality (4.2% versus 5.8%, P = 0.24) were not different between groups. The MIS cohort had a shorter hospital length of stay (3 days versus 6 days, P < 0.01) and less 30-day readmissions (4.4% versus 9.0%, P < 0.01). On multivariable Cox-proportional hazards analysis, undergoing an MIS resection was associated with decreased mortality (Hazard ratio [HR]: 0.83, 95% CI: [0.70-0.99], Fig. 4). After stratifying by clinical T-stage, there was no difference in survival among clinical T-stage I (HR: 0.71, 95% CI: [0.38-1.36]), II (HR: 0.89, 95% CI: [0.67-1.19]), III (HR: 1.31, 95% CI [0.88-1.96]), or IV (HR: 0.61, 95% CI: [0.30-1.24]) disease (Fig. 5).
The open cohort was more likely to have clinical stage IV disease (38.9% versus 22.3%, P < 0.01) and had higher rates of lymphovascular invasion (56.6% versus 47.9%, P < 0.01, Table 2). The open cohort was less likely to have a well differentiated tumor grade (7.7% versus 24.5%, P < 0.01). In addition, the open cohort had a high lymph node yield (1.71 versus 0.35, P < 0.01), but there was no difference in the
number of positive lymph nodes between approaches (0.99 versus 1.00, P = 0.43). Notably, there was no difference in rates of margin positivity between groups (22.3% versus 20.6%, P = 0.48).
Subset analysis: large (6 cm-9.9 cm) & giant (>10 cm) tumors
Among the 1183 total patients with tumors greater than 6 cm, 420 (35.5%) were large tumors (6 cm-9.9 cm) and 763 (64.5%) were giant ACC tumors (>10 cm). Of the 420 patients with large ACCs, 191 (45.5%) underwent MIS resection while 229 (54.5%) underwent open resection. Among patients with giant ACCs, 143 (18.7%) underwent MIS resection while 620 (81.3%) received an open operation. There was no difference in the utilization of the MIS approach for large ACC tumors after 2013 (46.3% versus 44.6%, P = 0.73), but there was an increase in the utilization of MIS for giant ACC tumors (23.8% versus 13.6%, P < 0.01). On Kaplan-Meier analysis, there was no difference in survival between recipients of an MIS resection versus open resection in large ACC (log-rank P = 0.66, Fig. 3B) or giant ACC tumors (log-rank P = 0.24, Fig. 3C). Similarly, on multivariable Cox proportional hazards analysis, there remained no differ- ence in survival between recipients of an MIS and open resection in large ACC (HR: 0.90, 95% CI: [0.68-1.21]) or giant ACC (HR: 1.08, 95% CI: [1.09-1.42]).
Discussion
The utilization of the MIS approach for adrenal tumors was first described 1992, and the evidence surrounding the onco- logic effectiveness of this approach remains controversial.20
Single-center retrospective case series have delivered conflicting results, some demonstrating decreased survival with an MIS approach,5,8,21 with others indicating no dif- ference in survival by operative technique.3,15,16 Indepen- dently, each of these studies represent high-volume, academic practices with experienced, senior surgeons. Our investigation adds to this literature by presenting a large and heterogenous population of patients, surgeons, and hospitals captured within the NCDB. The findings pre- sented here are more likely to reflect the current clinical practice in the United States as opposed to isolated aca- demic centers.
To our knowledge, the data presented in this investigation represents the largest and most recent cohort of resected ACC patients in the United States. We found an overall in- crease in MIS utilization for ACC without subsequent de- clines in patient survival on both univariable and multivariable analysis. After stratifying the study population by clinical T-stage, there was no difference in survival be- tween clinical stage I, II, III, or IV disease. Because guidelines often suggest a size cut-off for consideration of MIS versus open surgery, we isolated large tumors (6-10 cm) and giant tumors (>10 cm) and did not find any statistically significant differences in survival on univariable or multivariable analysis.
The most recent NCCN, American Association of Endocrine Surgeons/American Association of Clinical Endocrinologists ,
Clinical T stage I
Clinical T stage II
1.0
1.0
Cumulative survival
Cumulative survival
0.5
0.5
Surgical Approach
· MIS
Surgical Approach
· Open
HR: 0.71, 95% CI: [0.38-1.36]
· MIS
0.0
· Open
HR: 0.89, 95% CI: [0.67-1.19]
0
50
100
0.0
0
50
100
Time
Time
Clinical T stage III
Clinical T stage IV
1.0
1.0
Cumulative survival
Cumulative survival
0.5
0.5
Surgical Approach
Surgical Approach
· MIS
HR: 1.31, 95% CI: [0.88-1.96]
· MIS
HR: 0.61, 95% CI: [0.30-1.24]
0.0
Open
0.0
Open
0
50
100
0
50
100
Time
Time
European Society of Endocrine Surgeons , and European Network for the Study of Adrenal Tumors guidelines uni- formly recommend open adrenalectomy in all adrenal tumors with a high suspicion of malignancy.9,22,23 However, the NCCN and ESSES/European Network for the Study of Adrenal Tu- mors guidelines do offer nuance with regards to tumor size, and suggest adrenal tumors >6 cm should not be attempted laparoscopically.23 We found that there was no difference in survival amongst patients who underwent MIS versus open surgery for tumors >6 cm or >10 cm. This finding is supported by previous studies which also suggest tumor size is less important than tumor invasion with respect to survival.15,24 Taken together, our data suggests the size of the adrenal tumor is not the primary driver of decreased survival in adrenocortical carcinoma, and an MIS approach can be considered without a significant independent risk of decreased survival compared to an open approach. These findings can be used to add clarity to national guideline recommendations.
This investigation has several limitations. Given the retrospective nature of the study, it is subject to significant selection bias of the operating surgeon. Patients who
underwent an MIS approach for ACC resection were more likely to have less disease burden than those who were initially selected for an open resection. We are unable to determine if the intent of the procedure was for malignant or benign disease at the outset. Therefore, we cannot comment on the surgeon’s pre-test probability for malignancy. How- ever, given that current guidelines recommend open surgery for known or suspected ACC, it is likely that the surgeons utilizing an MIS approach did not suspect ACC before sur- gery. It is notable that a significant proportion of MIS surgery was performed for adrenal tumors >6 cm in size despite existing guideline recommendations. The observation that MIS surgery was frequently performed for tumors >6 cm in size in spite of guideline recommendations, together with the finding that survival was equivalent independent of size or approach, suggests that appropriate selection by surgeons likely plays a significant role. A second major limitation of the NCDB, is the lack of disease recurrence information in the dataset. Although the database is robust with respect to overall survival, we are unable to assess the differing rates of local recurrence or peritoneal recurrence in this population. A third limitation is the lack of data regarding tumor capsule
| Table 2 - Oncologic details stratified by initial operative approach. | |||
| Characteristic | MIS (n = 501, 33.8%) | Open (n = 982, 66.2%) | P-value |
| Tumor size, mm, median [IQR] | 75 [52-105] | 120 [80-165] | <0.01 |
| Clinical stage, n (%) | <0.01 | ||
| Stage I | 83 (23.5%) | 52 (6.9%) | |
| Stage II | 172 (48.6%) | 324 (43.2%) | |
| Stage III | 43 (12.2%) | 123 (16.4%) | |
| Stage IV | 56 (15.8%) | 251 (33.5%) | |
| Lymphovascular invasion, y, n (%) | 189 (47.9%) | 440 (56.6%) | <0.01 |
| Tumor grade, n (%) | <0.01 | ||
| Well differentiated | 25 (24.5%) | 16 (7.7%) | |
| Moderately differentiated | 12 (11.8%) | 37 (17.8%) | |
| Poorly differentiated | 39 (38.2%) | 97 (46.6%) | |
| Undifferentiated | 26 (25.5%) | 58 (27.9%) | |
| Pathologic stage, n (%) | <0.01 | ||
| Stage I | 39 (13.5%) | 19 (2.8%) | |
| Stage II | 109 (37.7%) | 233 (34.0%) | |
| Stage III | 82 (28.4%) | 167 (24.3%) | |
| Stage IV | 59 (20.4%) | 267 (38.9%) | |
| Margin positive, y, n (%) | 100 (22.3%) | 180 (20.6%) | 0.48 |
| Number of lymph nodes examined, mean ± sd | 0.35 ± 2.25 | 1.71 ± 4.65 | <0.01 |
| Number of positive lymph nodes, mean ± sd | 1.0 ± 2.25 | 0.99 ± 3.00 | 0.43 |
| Length of stay, days, median [IQR] | 3 [1-5] | 6 [4-8] | <0.01 |
| 30-day readmission, y, n (%) | 22 (4.4%) | 88 (9.0%) | <0.01 |
| 30-day mortality, y, n (%) | 5 (1.2%) | 22 (2.6%) | 0.10 |
| 90-day mortality, y, n (%) | 18 (4.2%) | 49 (5.8%) | 0.24 |
| MIS = minimally invasive surgery. | |||
spillage during MIS resection. The NCDB does provide data on the conversion rate from MIS to open (79/501, 15.8% in our study population), but we are unable to discern why the case was converted. Lastly, although our results suggest a lack of an association between MIS resections and decreased sur- vival, these findings must be validated by prospective, multicenter clinical trials.
Conclusions
This investigation of 1483 resected ACC patients across the United States found no difference in overall survival between patients who underwent MIS versus open resection irre- spective of tumor size >6 cm. Our findings suggest that MIS adrenalectomy should be considered, irrespective of tumor size, for carefully selected lesions deemed resectable by the surgeon.
Author Contributions
All authors (AMD; KMT; AG; ES; AMA; TMH) made substantial contributions to the conception and design, acquisition of data, and analysis and interpretation. Similarly, all authors (AMD; KMT; AG; ES; AMA; TMH) participated in drafting and critical revisions and gave final approval for the manuscript to be published.
Disclosure
None declared.
Funding
The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
Meeting Presentation
Academic Surgical Congress for the Association of Academic Surgeons, 2022.
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