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Surgical resection for adrenocortical carcinoma: Current trends affecting survival
Monali Shah1 D | Rachel E. NeMoyer MD, MPH2 Richi Kashyap3
Yong Lin PhD4 Juan Sarmiento MD5 I David A. Kooby MD5 İD
|
Shishir K. Maithel MD5 İD
| Theresa W. Gillespie PhD5 Amanda M. Laird MD2
Mihir M. Shah MD5 İD
1Department of Medicine, Philadelphia College of Osteopathic Medicine, South Georgia, Philadelphia, Pennsylvania, USA
2Department of Surgery, Division of Surgical Oncology, Rutgers Cancer Institute of New Jersey, Rutgers Robert Wood Johnson Medical School, New Brunswick, New Jersey, USA
3Department of Medicine, Maulana Azad Medical College, Delhi, India
4Department of Biostatistics and Epidemiology, Division of Biometrics, Rutgers Cancer Institute of New Jersey, School of Public Health, Rutgers University, Piscataway, New Jersey, USA
5Department of Surgery, Division of Surgical Oncology, Emory University School of Medicine, Atlanta, Georgia, USA
Correspondence
Amanda M. Laird, Division of Endocrine Surgery, Rutgers Cancer Institute, 195 Little Albany St, New Brunswick, NJ 08901, USA. Email: amanda.laird@cinj.rutgers.edu
Mihir M. Shah, Division of Surgical Oncology, Emory University School of Medicine/Winship Cancer Institute, 5665 Peachtree Dunwoody Rd, Oncology Suite, 2nd Floor, Atlanta, GA 30342, USA.
Email: mihir.m.shah@emory.edu
Abstract
Introduction: Adrenocortical carcinoma (ACC) is associated with a poor prognosis. We reviewed the National Cancer Database (NCDB) to analyze the prognostic factors in surgically resected ACC patients and the association of surgical approaches with overall survival (OS).
Methods: A retrospective NCDB (2004-2014) review of patients undergoing curative-intent surgical resection for ACC was performed. Effects of patient demographics, tumor characteristics, histopathology, and perioperative course on OS were analyzed. Log-rank statistics were used to associate clinical variables with OS. The multivariable Cox proportional hazard model included only statistically significant variables.
Results: A total of 1599 patients with ACC were included. A majority of patients were female (60.73%) and presented with a Charlson-Deyo score of zero (75.42%). A majority of the ACC cases were Grade 3 (45.69%), and almost a third (30.64%) underwent margin-positive resections. Univariate analysis demonstrated a decrease in OS associated with increasing age and comorbidities. A negative resection margin and lack of lymphovascular invasion predicted better OS. Multivariable analysis showed that age, grade, surgical resection margins, and hospital length of stay were associated with OS.
Conclusions: Advanced age, grade, presence of lymphovascular invasion, and positive surgical margins predicted a worse overall survival for adrenocortical cancer in our analysis. Resection with negative margins improves outcomes.
KEYWORDS
NCDB, retrospective, systemic therapy
1 INTRODUCTION |
Adrenal tumors are common, affecting between 3% and 10% of the population. However, adrenocortical carcinoma (ACC) is a very rare form of adrenal cancer, with an incidence of 0.7-2 people per million.1,2 ACC is an aggressive endocrine malignancy, second only to anaplastic thyroid cancer.1,3 It is more common in females compared with males (1.5:1), with a median diagnosis age of 46 years.1,3,4 Unfortunately, ACC is associated with a poor prognosis, as the majority of the patients present at advanced stages, with 50%-70% of the patients presenting with distant metastatic disease.1,3,5 ACC carries a median OS of 60%-80% in patients with ACC Stage 1, and an overall 5-year OS rate of 13% in patients with ACC Stage 4.º Approximately 40%-60% of the patients present with symptomatic hormone excess, including glucocorticoid, mineralocorticoid, and androgenic excess. About 30% of the patients may have abdominal symptoms due to mass effects from the tumor, and up to 20% of the patients are diagnosed incidentally.2,4
The treatment approach for ACC includes surgical resection and systemic therapy. According to the National Comprehensive Cancer Network Guidelines for Neuroendocrine and Adrenal Tumor Man- agement, resection may be considered for a metastatic adrenal carcinoma if greater than 90% of the tumor and metastases can be removed. According to Tran et al.,7 surgery for ACC can offer a 25% chance of 5-year survival, and a 1 in 15 chance of 10-year survival. Otherwise, systemic therapy should be pursued in the metastatic setting.8 Unfortunately, tumor recurrence is a common scenario, occurring in up to 80% of the patients, with survival benefit in patients undergoing further surgical resection of recurrent dis- ease.2,3,5 Controversy exists regarding debulking for hormonal excess in metastatic disease and requires patient-specific discussions on treatment.2,5,9 Poor prognostic variables encompass incomplete surgical resection, advanced stage, and pathological grade.1,5,10,11 Additional variables such as sex, hormonal hypersecretion, large tumor size, and advancing age are associated with a worse prognosis.1,4,12 Currently, these prognostic variables are mainly defined in studies with smaller sample sizes.
Few studies have described and analyzed treatment patterns for ACC in the United States.2,13,14 This study utilizes the National Cancer Data Base (NCDB) to assess patients who undergo resection for ACC and determine the prognostic variables associated with overall survival (OS). Current treatment approaches in the United States and factors associated with improved OS after resection of ACC are also analyzed.
2 METHODS |
A retrospective review of patients undergoing curative-intent surgery for ACC was performed using the NCDB from 2004 to 2014. The NCDB is a joint project of the Commission on Cancer of the American College of Surgeons and the American Cancer Society. The data used in the study were derived from a deidentified NCDB
file. The American College of Surgeons and the Commission on Cancer have not verified and are not responsible for the analytic or statistical methodology employed, or the conclusions drawn from these data by the investigators. The Rutgers Institutional Review Board (IRB) reviewed this study and deemed it exempt from IRB approval.
Primary site (C74.0-C74.9) and histology codes were used to select patients with ACC, based on the International Classification of Diseases for Oncology, third edition (ICD-0-3.1). Patients were excluded if they did not undergo surgery, had missing data or underwent palliative surgery. We analyzed patient demographics, tumor characteristics, operative histopathology, and perioperative course.
Kaplan-Meier plots for OS were calculated. First, the univariate cox proportional hazard model was used to test the association of clinical variables with OS. The multivariable Cox proportional hazard model included only clinical variables that were significantly associated with OS in univariate analyses. However, surgical approach and lymphovascular invasion were purposely not included in the multivariable analysis due to the resultant significant decrease in a number of analyzed patients, as NCDB accounted for these variables only since 2010. A significance level of 0.05 was used for all the tests. Statistical calculations were carried out using SAS software version 9.4 (SAS Institute, 2018).
3 RESULTS |
A total of 1599 patients with ACC met inclusion criteria (Figure 1). The median age at diagnosis was 52.8 years (range: 18-89 years). The median OS was 49 months (95% confidence interval: 42-56 months) (Figure 2). There was a higher proportion of female patients (60.73%). Approximately 75.42% of patients had a Charlson-Deyo score of 0, suggesting no limiting comorbidities. The average tumor size was 11.5 ± 2.3 cm. The majority of ACC were grade 3 (45.69%). Most patients (69.04%) underwent an open or unspecified approach for tumor resection, and 18.8% of patients underwent a laparoscopic approach. Almost one-third of patients (30.64%) were margin- positive on resection. Most patients (46.96%) were discharged between postoperative Days 4-7 (Table 1).
Univariate analysis was then performed to identify factors associated with worse OS (Table 2). Patients under the age of 55 did better than those who were older. Patients 55-75 were 36% more likely to die and those over 75 were 87% more likely to die compared to younger patients (p < 0.0001). Patients with a Charlson-Deyo score of 1 (hazard ratio [HR] 1.399) and 2 or higher (HR 1.669) did worse than those with a score of 0 (p < 0.0001). Patients with Grade 3 and 4 tumors also had worse OS (HR 3.028, p = 0.0002 and HR 2.633, p =0.0018, respectively), compared to Grade 1. On univariate analysis, those with negative margins had improved OS compared with those with positive margins (p < 0.0001) as did those with no lymphovascular invasion present (p = 0.0005). Patients with a tumor size ≤ 5 cm were associated with an improved
|
Journal of WILEY- SURGICAL ONCOLOGY
NCDB ACC Cases: Histology 8370 (2004-2014) n = 3,018
Excluded: Other primary sites (n=13) Patients without surgery (n=892)
Patients receiving palliative care (n=82)
Patients with more than one malignant primary tumor (n=317)
Patients with no surgical procedure of primary site performed at facility (n=115)
Total NCDB ACC Cases for this study: n = 1,599
Product-Limit Survival Estimate
1.0
+ Censored
0.8
Survival Probability
0.6
0.4
0.2
0.0
0
50
100
150
Last Contact or Death, Months from Dx
OS compared with patients with a tumor size ≥ 15 cm (p = 0.0028, HR = 0.669). An increase in length of hospital stay predicted a worse OS. Compared with patients with a hospital stay of less than 4 days, patients with hospital length of stay 4-7 days and > 7 days presented with a worse outcome (HR 1.284, p =0.0058 and HR 2.166, p < 0.0001, respectively). When robotic or laparoscopic surgery was converted to an open procedure, OS was worse (p = 0.0550, robotic and p = 0.0313, laparoscopic). Interestingly, surgery alone without the use of adjuvant systemic therapy, compared to receipt of adjuvant systemic therapy, was associated with improvement in OS nearly reaching statistical significance on univariable analysis (p = 0.0567, HR = 0.867). Laterality, patient sex or race, year of diagnosis, and receipt of radiation therapy did not demonstrate a statistically significant association with OS. The complete list of variables can be found in Table 2.
We then performed multivariable analysis to determine the variables that independently affect OS (Table 3). Age, grade, surgical resection margins, and hospital length of stay maintained statistical
significance. On multivariable analysis older age, higher grade, longer postoperative length of stay, and positive resection margins were all predictive of worse OS (Table 3).
4 DISCUSSION |
These data identify prognostic variables in patients who undergo resection for ACC. The outcome of patients undergoing surgery for ACC remains poor with a median OS of approximately four years. Increasing age was independently associated with worse OS. Histopathologic features traditionally associated with poor prognosis for solid organ malignancies include advanced grade and presence of lymphovascular invasion-this was true for our study as well, where Grade 3 and Grade 4 tumors predicted worse OS. The presence of lymphovascular invasion is associated with a worse disease-specific survival, as proven by Poorman et al.15 However, presence of lymphovascular invasion did not influence survival in patients with
| N | Percent | |
|---|---|---|
| <55 years old | 863 | 53.97 |
| 55-75 years old | 608 | 38.02 |
| ≥75 years old | 128 | 8.01 |
| Charlson-Deyo Score 0 | 1206 | 75.42 |
| Charlson-Deyo Score 1 | 300 | 18.76 |
| Charlson-Deyo Score >1 | 93 | 5.82 |
| Northeast | 278 | 21.63 |
| South | 441 | 34.32 |
| Midwest | 347 | 27.00 |
| West | 219 | 17.04 |
| White | 1383 | 87.26 |
| Black | 139 | 8.77 |
| Other Race | 63 | 3.97 |
| Male | 628 | 39.27 |
| Female | 971 | 60.73 |
| Grade 1 | 41 | 11.08 |
| Grade 2 | 77 | 20.81 |
| Grade 3 | 169 | 45.68 |
| Grade 4 | 83 | 22.43 |
| Negative surgical margins | 1109 | 69.36 |
| Positive surgical margins | 490 | 30.64 |
| Postoperative length of stay ≤ 3 days | 423 | 28.26 |
| Postoperative length of stay 4-7 days | 703 | 46.96 |
| Postoperative length of stay ≥ 7 days | 371 | 24.78 |
| <50 mm tumor | 164 | 10.85 |
| 50 to < 150 mm tumor | 970 | 64.20 |
| ≥150 mm tumor | 377 | 24.95 |
| No radiation therapy | 1353 | 85.80 |
| Radiation therapy after surgery | 224 | 14.20 |
| No systemic therapy given | 825 | 63.07 |
| Systemic therapy given before surgery | 13 | 0.99 |
| Systemic therapy given after surgery | 470 | 35.93 |
| No lymphovascular invasion | 256 | 44.99 |
| Lymphovascular invasion present | 313 | 55.01 |
| Robotic-assisted procedure | 46 | 6.42 |
| Robotic procedure converted to open | 4 | 0.56 |
| Laparoscopic procedure | 135 | 18.83 |
| Laparoscopic procedure converted to open | 37 | 5.16 |
| Open/unspecified approach | 495 | 69.04 |
T1 or T4 disease.15 Surgical resection margin is one of the potentially modifiable variables that independently affect OS in patients under- going surgical resection. Patients should be carefully selected if laparoscopic or robotic surgery is planned in an effort to later avoid conversion to open surgery as these data show worse outcomes compared to planned open surgery. Our study also demonstrated that an increasing length of stay was associated with worse OS outcomes for the patient, a correlation that is often seen. A longer hospital length of stay is associated with adverse health outcomes, including the increased risk of nosocomial infections and declines in physical and cognitive function. Interestingly, in our study, systemic therapy did not improve the OS of these patients, most likely indicating the advanced nature of the disease at presentation.
Patients undergoing laparoscopic adrenalectomy may be more likely to recur with lesions surrounding the primary tumor site after the initial surgery.16 Moreover, a retrospective research study published in 2013 showed that patients undergoing an open operation for ACC had a lower rate of positive margins than those receiving laparoscopic resection.17 The OS and recurrence-free survival rates of patients who underwent open adrenalectomy were also shown in that study to be significantly longer compared with other surgical approaches. Our study showed an association with worse OS for patients converted from minimally invasive to an open operation. It is unclear if this is due to selection of patients with advanced disease requiring conversion or technical difficulty during the operation. However, minimally invasive completion of the operation did not appear to be inferior to the open approach. It is vital to prolonging the disease-free survival after primary surgery because once ACC recurs, the options and therapeutic effects of sequential treatments are very limited.16
Surgical resection in the setting of ACC recurrence remains a potentially curative option. However, long-term survival after repeat resection for recurrent ACC is beneficial only if the tumor is solitary if the patient has had a disease-free interval greater than 12 months, and if the recurrence is locoregional or pulmonary.18 Due to high rates of recurrence (60%-70%), adjuvant therapies are often used after surgical resection.8 However, limited data is available regarding the use of adjuvant systemic therapy in patients with ACC. Systemic adjuvant therapy approaches include the routine use of mitotane, mitotane with chemotherapy, and radiation therapy. A combined regimen including etoposide, doxorubicin, and cisplatin with mitotane (EDP-mitotane) is considered the most effective chemotherapy for ACC patients.19 Although a significant improvement in OS is not proven to be achieved with EDP-mitotane, it has higher antitumor efficacy than other drugs.20,21 Our review of the NCDB showed that patients who received surgery without postprocedural adjuvant systemic therapy were associated with an improvement in OS, probably related to selection of patient who receive adjuvant therapy. A recent analysis of multiple cohort studies showed a reduction in the likelihood of recurrence and prolonged time to recurrence when adjuvant radiation was used in ACC without improvement in OS.15
| Variable | Class value | Compared with | p Value | Hazard ratio |
|---|---|---|---|---|
| Age | 55-75 years | <55 years | <0.0001 | 1.358 |
| Age | ≥75 years | <55 years | <0.0001 | 1.872 |
| Charlson-Deyo Score | 1 Comorbidity | No comorbidities | <0.0001 | 1.399 |
| Charlson-Deyo Score | 1+ Comorbidities | No comorbidities | <0.0001 | 1.669 |
| Facility location | Midwest | West | 0.5321 | 0.931 |
| Facility location | North East | West | 0.6390 | 0.946 |
| Facility location | South | West | 0.4322 | 0.917 |
| Race | Black | White | 0.2103 | 1.155 |
| Race | Other | White | 0.8473 | 0.965 |
| Sex | Males | Females | 0.9902 | 0.999 |
| Grade | 2 | 1 | 0.3706 | 1.347 |
| Grade | 3 | 1 | 0.0002 | 3.028 |
| Grade | 4 | 1 | 0.0018 | 2.633 |
| Surgical margins | Negative | Positive | <0.0001 | 0.454 |
| Postoperative length of stay | 4-7 Days | <4 days | 0.0058 | 1.284 |
| Postoperative length of stay | ≥7 Days | <4 days | <0.0001 | 2.166 |
| Tumor size | 50 to <150 mm | ≥150 mm | 0.1685 | 0.896 |
| Tumor size | <50 mm | ≥150 mm | 0.0028 | 0.669 |
| Year of diagnosis | 2004-2009 | 2010-2014 | 0.2366 | 1.090 |
| Radiation therapy | No radiation therapy | Radiation therapy after surgery | 0.7428 | 1.034 |
| Systemic therapy | No systemic therapy | Systemic therapy after surgery | 0.0567 | 0.860 |
| Systemic therapy | Systemic therapy before surgery | Systemic therapy after surgery | 0.9198 | 0.962 |
| Lymphovascular invasion | No lymphovascular invasion | Lymphovascular invasion present | 0.0005 | 0.640 |
| Surgical approach | Robotic-assisted surgery | Open/unspecified | 0.4720 | 0.830 |
| Surgical approach | Robotic surgery converted to open | Open/unspecified | 0.0550 | 3.057 |
| Surgical approach | Endoscopic/laparoscopic surgery | Open/unspecified | 0.2758 | 0.847 |
| Surgical approach | Endoscopic/laparoscopic surgery converted to open | Open/unspecified | 0.0313 | 1.621 |
Only a few studies analyze the treatment patterns of ACC in the United States using the NCDB. Tella et al.22 evaluated predictors of OS in ACC by focusing on tumor grades, baseline Charlson-Deyo scores, and stage of diagnosis. Similar to our findings, they reported that ACC is more common in women, and that older age at diagnosis and more advanced stage of disease at diagnosis were associated with a shorter OS. However, they did not provide data regarding tumor size or postoperative length of stay. Wang et al.23 described the prognostic factors of ACC with data from the Surveillance Epidemiology and End Results (SEER) database. The SEER database allowed the analysis of 749 patients between the years 1973 and 2014; however, a majority of the study focused on the white race demographic (84.4%). Furthermore, their treatment modality variable did not specify the surgical approach for the
tumor site. The study concluded that patients with younger age, surgical resection of the primary lesion, receipt of chemotherapy, and early tumor stages were associated with an improvement in OS, with tumor stage being the dominant predictor of OS. The features of patients who underwent synchronous versus metachronous metastasectomy were compared by Prendergast et al.24 Their study highlighted that select patient with metastatic adrenocortical carcinoma may benefit from surgical resection, and that patients undergoing metachronous metasta- sectomy will have a higher survival benefit than patients undergoing synchronous metastasectomy. Their study of 84 patients proved that the metachronous group had a prolonged median survival after metasta- sectomy (36.9 vs. 17.3 months, p = 0.007). However, their study did not encompass data comparing variables used in our study.
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| Parameter | Class value | Compared with | p Value | Hazard ratio |
|---|---|---|---|---|
| Age | 55-75 | <55 years | 0.0511 | 1.377 |
| Age | ≥75 | <55 years | 0.0019 | 2.325 |
| Charlson-Deyo score | 1 comorbidity | No comorbidities | 0.0538 | 1.478 |
| Charlson-Deyo score | 1+ comorbidities | No comorbidities | 0.8654 | 1.048 |
| Grade | 2 | 1 | 0.9134 | 1.040 |
| Grade | 3 | 1 | 0.0010 | 2.897 |
| Grade | 4 | 1 | 0.0066 | 2.525 |
| Surgical margins | Negative | Positive | 0.0002 | 0.547 |
| Postoperative length of stay | 4-7 Days | <4 days | 0.0514 | 1.529 |
| Postoperative length of stay | ≥7 Days | <4 days | 0.0001 | 2.475 |
| Tumor size | 50 to <150 mm | ≥150 mm | 0.6391 | 1.090 |
| Tumor size | <50 mm | ≥150 mm | 0.5011 | 0.784 |
Limitations of our study include its retrospective study design which is vulnerable to misclassification bias, coding error, and missing registry-based data.25 The NCDB does not contain data for specific variables of interest for systemic therapy approaches such as dose, type, and duration of chemotherapy and analysis of the effect of a particular therapy on disease-specific survival. Data on recurrence in the NCDB is not included, and OS encompasses OS only, not disease- specific survival. While the data set includes samples from more than 1500 institutions across the United States, which leads to larger samples and strengthens the statistical analysis resulting from real- world data, the differences in histopathologic interpretation and margin measurements of ACC specimens by different pathologists across the various institutions may have occurred leading to inconsistencies. Furthermore, the NCDB not have sufficient data regarding cortical-secreting status of ACC. It has been found that cortisol secretion is associated with an increased risk of postoperative morbidity, and that cortisol secretion is independently associated with shorter recurrence-free survival.26 Therefore, the cortisol-secreting status of the ACC specimens can have an impact on survival data.
5 CONCLUSION |
Adrenocortical carcinoma portends a poor prognosis. Margin- negative surgical resection is associated with an improvement in overall survival. As frequently seen, the presence of a high-grade adrenocortical carcinoma and lymphovascular invasion are associated with a poor prognosis for patients with adrenocortical carcinoma. The median overall survival rate for adrenocortical carcinoma remains poor, even in patients undergoing surgical resection without limiting comorbidities. Careful attention should be paid to achieving a negative surgical margin through appropriate oncologic resection as this may lead to improved outcomes, including overall survival.
DATA AVAILABILITY STATEMENT
The authors confirm that the data supporting the findings of this study are available within the article, its supplementary materials, and the National Cancer Database.
ORCID
Monali Shah (D http://orcid.org/0000-0002-2427-9988
David A. Kooby (D https://orcid.org/0000-0001-8694-0455
Shishir K. Maithel D https://orcid.org/0000-0002-3591-8925
Mihir M. Shah İD https://orcid.org/0000-0002-4665-5534
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How to cite this article: Shah M, NeMoyer RE, Kashyap R, et al. Surgical resection for adrenocortical carcinoma: current trends affecting survival. J Surg Oncol. 2022;125:1224-1230. doi:10.1002/jso.26845