A SERVICES . USA
HHS Public Access Author manuscript Am J Surg. Author manuscript; available in PMC 2023 June 17.
Published in final edited form as: Am J Surg. 2022 October ; 224(4): 1090-1094. doi:10.1016/j.amjsurg.2022.05.033.
Surgical outcomes and survival of adrenocortical carcinoma between children and adults
Adesola C. Akinkuotua,*, Alyssa Peaceª, Ugwuji N. Maduekweb, Andrea A. Hayesa
ªDivision of Pediatric Surgery, Department of Surgery, University of North Carolina Chapel Hill, Chapel Hill, NC, USA
bDivision of Surgical Oncology & Endocrine Surgery, Department of Surgery, University of North Carolina Chapel Hill, Chapel Hill, NC, USA
Abstract
Introduction: Adrenocortical carcinoma (ACC) is associated with poor outcomes. We compared surgical outcomes between children and adult; and identified factors independently associated with survival.
Methods: Using the National Cancer Database, children and adults with ACC who underwent surgery between 2004 and 2016 were identified. We compared outcomes and survival between groups. Cox regression analysis was performed to identify predictors of survival.
Results: Of 2553 patients, 2.8% were children. A higher proportion of children were Hispanic (19.1%vs.6.6%) and covered by government insurance (45.1%vs.35.8%) than adults. More pediatric patients received lymphadenectomy and chemotherapy than adults. Pediatric patients had better survival at 1 -(91.4%; 95%CI: 81.2%- 96.0% vs.79.6%; 95%CI: 77.9%-81.1%) and 5-years (60.6%; 95%CI:47.5%-71.3% vs.44.9%; 95%CI 42.7%-47.0) (p =0.0016). Age≥18 (HR: 2.21(1.50-3.27)), metastatic disease at diagnosis (HR: 3.51(3.04-4.04)), and receipt of lymphadenectomy (HR: 1.30(1.14-1.48)) were independently associated with worse survival.
Conclusions: Children with ACC had better survival than adults. Factors independently associated with worse survival included older age, metastatic disease, and receipt of lymph node surgery.
Keywords
Adrenocortical carcinoma; ACC; Pediatric cancer
1. Introduction
Adrenocortical carcinoma (ACC) is a rare, endocrine malignancy that accounts for approximately 0.2% of all childhood malignancies.1 It has an incidence of 0.2-0.3 cases
“Corresponding author. Division of Pediatric Surgery, Houpt Physicians’ Building, 170 Manning Drive, Chapel Hill, NC, 27599, USA. adesola_akinkuotu@med.unc.edu (A.C. Akinkuotu).
per million children per year and a bimodal age distribution, with the majority of pediatric cases occurring before the age of five years.2,3 Despite the rarity of ACC, its incidence is associated with a notable pattern, with southern Brazil having an incidence that is more than ten times the worldwide incidence, which has been associated with a high frequency of a germline mutation in the TP53 gene(1, 3). Although the majority of ACC in children are sporadic in nature, individuals with genetic conditions including Li-Fraumeni syndrome, Beckwith-Wiedemann syndrome, and familial adenomatous polyposis are at increased risk for developing ACC.1,4 Importantly, the majority of pediatric ACC is associated with a germline TP53 mutation1,3
In the United States, management of pediatric ACC is largely dependent on disease stage as proposed by Sandrini et al.(5), with surgical resection as the mainstay of therapy. The use of adjuvant therapies in the management of pediatric ACC remains variable. A recent protocol, ARAR0332, by the Children’s Oncology Group (COG) advocates adjuvant use of a regimen containing mitotane, cisplatin, etoposide, and doxorubicin in children with incomplete resections, tumor spillage, and distant metastasis.6 Given that most children with ACC have a TP53 mutation, which predisposes to a higher risk of other malignancies, radiation therapy is often avoided. Despite the multimodal treatment strategy that is used, ACC is associated with an aggressive clinical course and high mortality rate in children and adults. Recent studies in adults undergoing complete surgical resection of ACC have reported 5-year survival between 13 and 80%,2,7 while studies in children have demonstrated 5-year survival between 50 and 90%, depending on the extent of disease.4,8,9 Factors that have been associated with increased risk of recurrence include age at time of presentation, tumor size, complete surgical resection, and presence of metastatic disease.10,11 These studies have largely been limited by the fact that they have been performed using single institution reviews.
The purpose of this study was to compare outcomes of pediatric and adult patients who underwent surgical resection of ACC, using a large, national database. Given that previous, single-institution studies have demonstrated better survival, we hypothesized that pediatric patients would have better outcomes than adults in a nationally-representative sample. We also sought to identify factors that were independently associated with survival.
2. Methods
All patients with a diagnosis of ACC who underwent definitive surgery between 2004 and 2016 were identified from the National Cancer Database (NCDB). The NCDB is a clinical oncology database that is jointly sponsored by the American College of Surgeons Commission on Cancer and the American Cancer Society. The database tracks outcomes of patients with malignancies across more than 1500 Commission on Cancer-accredited facilities, representing a majority of newly diagnosed malignancies in the United States.12
Patients with International Classification of Diseases for Oncology morphology code for adrenocortical carcinoma (8370 and 8373) with primary codes for the adrenal gland (C74.0) who underwent any surgical resection were included in the analysis. Pediatric patients were defined as those less than 18 years of age and adults were those ≥18 years of age. Patients
with missing data about surgical treatment, receipt of chemotherapy, and radiation were excluded from the analysis. The study was reviewed and deemed exempt by the University of North Carolina Institutional Review Board.
Patient demographics including sex, race, insurance status, zip-code linked median income and educational attainment according to the 2012 American Community Survey, and baseline health status using the Charlson-Deyo Score, as a marker of health status were compared between groups. Charlson-Deyo score was dichotomized into either “no comorbidities”, Charlson-Deyo score of 0, or “comorbidities”, Charlson-Deyo score ⇒ 1. Cancer-related characteristics including primary tumor site and size were compared between groups. Tumor size was dichotomized into lesions <5 cm and those ≥ 5 cm, due to increasing concern for malignancy once larger than 5 cm. Surgical outcomes of interest included type of surgery performed, margin status, hospital length of stay, 30-day readmission rates, 30-and 90-day mortality rates compared between groups.
Descriptive statistics were calculated for patient demographics, tumor characteristics, and outcomes, using chi-squared tests, Wilcoxon-rank sum or ANOVA as appropriate, based on the age grouping. Continuous variables are reported as medians with interquartile ranges. Overall survival was calculated at 1- and 5-years using Kaplan-Meier method. We also performed a multivariate Cox regression analysis of overall survival. Independent covariates included in the analysis included age, health status, insurance status, presence of metastatic disease at diagnosis, receipt of lymph node surgery, receipt of chemotherapy, and receipt of radiation therapy. Insurance status was dichotomized to private or not private for the regression analysis. We then performed a multivariate Cox regression analysis for pediatric patients, which included the aforementioned covariates. Age was dichotomized to age<5 and ≥ 5 years of age. Statistical analyses were carried out using STATA version 16.1 (STATA, College Station, TX, USA). A p-value <0.05 was considered statistically significant.
3. Results
There was a total of 3621 patients with malignant adrenocortical carcinoma; 2553 underwent surgical resection and were included in the analysis. Of the patients included in the analysis, 71 (2.8%) were pediatric patients and 2482 (97.2%) were adults.
Table 1 illustrates the comparison between pediatric and adults based on demographic factors and baseline tumor characteristics. There was no difference in the proportion of female patients between groups. A higher proportion of pediatric patients were Hispanic (19.1% vs.6.6%) and covered by Medicaid/Medicare (43.7% vs. 34%) compared to adult patients. Pediatric patients were healthier, with no comorbidities, compared to adult patients (91.5% vs. 74.3%). There were no significant differences in tumor laterality or size between groups.
Table 2 compares treatment strategies and surgical outcomes between pediatric and adult patients. There was no difference in the type of surgery that patients underwent, between groups. A significantly higher proportion of pediatric patients received regional lymph node surgery (36.9% vs. 16.6%; p < 0.001) and chemotherapy (57.15 vs. 40.4%; p = 0.004%)
compared to adult patients. More adults were managed with external beam radiation therapy compared to pediatric patients (15.5% vs. 7.2%; p = 0.04). Pediatric patients had significantly longer hospital length of stay (median (IQR): 64-9 vs. 53-7 days; p = 0.011) and 30-day readmission rates (15.7% vs. 6.5%; p = 0.003). There was no significant difference in 30- and 90-day mortality between groups.
Fig. 1 illustrates the Kaplan-Meier analysis by age group. Pediatric patients had significantly better survival compared to adults at 1 (91.4%; 95%CI: 81.2%-96.0% vs. 79.6%; 95%CI: 77.9%-81.1%) and 5 years (60.6%; 95%CI:47.5%-71.3% vs. 44.9%; 95%CI 42.7%-47.0); p = 0.0016). On univariate analysis, health status, presence of metastatic disease, receipt of chemotherapy and radiation therapy were associated with decreased survival at 1- and 5-years (Table 3).
Using Cox regression analysis, factors independently associated with worsened survival included age≥18, HR: 2.21 (1.50-3.27), retroperitoneal lymph node removal, HR: 1.30 (1.14-1.48), and presence of metastatic disease at diagnosis, 3.51 (3.04-4.04). Private insurance was associated with improved survival (HR: 0.74(0.66-0.82)). Hispanic ethnicity and receipt of chemotherapy and external beam radiation were not independently associated with survival (Table 4).
In pediatric patients, we found that the presence of metastatic disease at diagnosis was the only factor independently associated with survival (HR: 3.02; 95% CI: 1.41-3.37). Receipt of lymph node surgery, chemotherapy, and radiation therapy were not independently associated with survival (Table 5).
4. Discussion
We found that pediatric patients had significantly improved survival when compared to adult patients. In our current study, we found that there were no significant differences in baseline tumor characteristics between children and adults. Despite this, children had significantly better overall survival compared to adults. This finding also held true on multivariate analysis in which age ≥ 18 was independently associated with decreased risk of survival. Interestingly, when we evaluated pediatric patients alone, age was not independently associated with risk of survival. Here we show a higher proportion of patients who were healthy, Hispanic, and covered by Medicaid; in the pediatric population when compared to adults. It is worth noting that we found a higher proportion of pediatric patients who were Hispanic, when compared to adults. This raises questions regarding potential associations between ethnicity and ACC itself or familial syndromes that may predispose to ACC. To date, there are no studies that have described any syndromes specific to Hispanic/ Latino ethnicity. However, it is well known and has well been described that the incidence of ACC in South America, particularly Brazil, has a many fold higher incidence of ACC than the United States.13,14 We believe that further studies are need to elucidate any potential differences in the incidence of ACC that may be related to the Hispanic ethnicity and predisposition to familial syndromes.
Although there were no differences in tumor size, stage, and presence of metastatic disease at presentation between groups, there was a higher proportion of pediatric patients who received regional lymph node surgery and chemotherapy when compared to adult patients. In general, pediatric patients do not have co-morbidities that may preclude them from having extensive surgery that includes the regional, retroperitoneal lymph nodes and/or chemotherapy. This may be the reason pediatric patients were more likely to have regional lymph node surgery and chemotherapy. Recently, the Children’s Oncology Group, COG, published results on the ARAR0332 protocol, which utilized a risk-based treatment strategy for pediatric patients with ACC. Pediatric patients with completely resected, small tumors (<100 g and <200 cm3) were treated with surgery alone, those with larger ( ≥100 g or ≥ 200 cm3) with surgery and retroperitoneal lymph node dissection (RPLND); those with presence of retroperitoneal lymph node involvement, tumor spillage or unresectable, residual microscopic or gross disease, or distant metastatic disease were treated with surgery, RPLND, cisplatin-based chemotherapy and mitotane6 The authors found that RPLND was not associated with an improvement in event-free survival in patients with large, completely resected ACC. However, the combination of surgery, RPLND, and adjuvant chemotherapy was associated with better outcomes in patients with retroperitoneal lymph node involvement, tumor spillage or unresectable, residual microscopic or gross disease. These findings led to the conclusion that although the role of RPLND in localized disease is unclear, it should be used in combination with surgery and adjuvant chemotherapy for pediatric ACC patients with tumor spillage or unresectable disease.6 Given the nature of the database used for this study, we are unable to delineate the extent to which each lymph node dissection was carried out. As such, it is difficult to ascertain the degree to which the extent of lymph node dissection may affect outcomes. Interestingly, Rodriguez-Galindo et al. recently noted in their publication that the median number of resected lymph nodes in the ARAR0332 protocol were low, likely indicating that the RPLND was not completed in their cohort. The authors also raise the critical point that RPLNDs are not often performed in pediatric patients, which could also explain low adherence to guidelines recommending its use in the management of pediatric ACC.6 Lastly, in our current study, we found that pediatric patients had longer hospital length of stay and 30-day readmission rates compared to adult patients. We posit that this difference in peri-operative outcomes could be attributed to children having had more extensive surgery including retroperitoneal node excision.
Although there is a paucity of studies that have directly compared outcomes between children and adults with ACC, our current study findings differ from a recent study by Sabaretnam et al., which did not demonstrate a difference in survival between adults and children.10 This is likely related to the fact that the current study composed of a nationally- representative cohort of patients, in comparison to the single institution study by Sabaretnam et al., which might not have been adequately powered to detect differences in survival between adults and children with ACC. Our findings are, however, similar to other studies that have identified increasing age as an independent predictor of survival in patients with ACC.11,15 This finding also held true in a study specifically looking at pediatric patients, in which age ≥ 4 was found to be independently associated with poor survival.9,16 Studies that have evaluated outcome of pediatric ACC have identified the bimodal age distribution, with one peak identified before the age of 5 years. In these studies, children <5 years of
age have been identified to have a more benign clinical course.16,17 Given that the median age at the time of presentation in our current pediatric cohort as 3 years of age, it is likely that the improved survival noted is due to biologically benign course, as has been previously suggested(16). The current study therefore adds to the body of literature highlighting the importance of age as a prognosticator for survival in patients with ACC. Importantly, the current study uses a cohort of patients that is reflective of a nationally-representative sample; and compares adults to children based not only on age, but other important tumor and disease characteristics.
Although not statistically significant, there was a higher proportion of pediatric patients with metastatic disease at the time of diagnosis. On survival analysis, the presence of metastatic disease was found to be independently associated with decreased survival. This finding is similar to findings of previous studies, which identified the presence of metastatic disease and higher disease stage as an independent prognostic factor for overall survival.4,15 Interestingly, the receipt of lymph node surgery was significantly associated with survival, but the receipt of chemotherapy or radiation therapy were not associated with survival. This finding, like that of the COG ARAR0332 protocol, suggests that there is a role for retroperitoneal lymph node dissection in a certain group of pediatric patients with ACC, when used in combination with surgery and adjuvant chemotherapy, for those with Stage III ACC.6 Our study finding does differ from that of the COG In that we did not find the receipt of chemotherapy to be associated with improved survival. This difference is likely due to the fact that COG protocol utilized a specific, risk-based protocol; which may not have been aligned with that used in all centers contributing to the NCDB.
Surgical resection remains the mainstay of therapy for ACC, with adjuvant therapies determined based on stage. We found that there was no difference in the surgical management strategy between children and adults. There was however a higher proportion of pediatric patient who received chemotherapy and lymph node surgery. This finding is in keeping with the fact that there was a higher proportion of pediatric patients with higher stage disease. Given the concerns about secondary malignancy due to radiation exposure in combination with genetic mutations, which are more common in pediatric patients with ACC, it was not surprising that significantly less children were managed with adjuvant radiation therapy when compared to adults. In our current cohort, we also found that the use of adjuvant radiation therapy was not independently associated with improved survival. It is worth noting however, that a recent, single-institution study demonstrated that adjuvant radiation improved recurrence-free and overall survival in ACC patients.18 Interestingly, the recent ARAR0332 protocol by the COG did not include the use of radiation therapy in the risk-based management protocol(6). Due to the fact that the management of ACC has largely been institution-dependent and guided by management strategies in adults, future studies are needed to evaluate the use of radiation therapy in children without genetic mutations who have ACC.
It is important to note that the current study has several limitations. Firstly, given that the data used is registry-based and retrospective, we are limited by missing datapoints. Secondly, the data in the NCDB is collected on a voluntary basis and only accounts for about a third of hospitals in the United States, thus the generalizability of our findings may
be limited to centers similar to those in the NCDB. Furthermore, we are unable to elucidate datapoints including patient presentation and family history. Given that ACC has been associated with genetic syndromes and can be functioning or non-functioning with respect to hormone secretion, it is likely that these datapoints would be important with regard to getting a more complete picture of the course of ACC. We suspect that the presence of genetic syndromes and functioning lesions likely lead to earlier detection, thus potentially causing a lead time bias, which would potentially affect our survival analysis by increasing the length of survival. Given that we do not have data regarding these factors in both adults and children, we believe that this potential for bias is non-differential. Lastly, it is important to note that data regarding survival in the NCDB is reflective of all-cause survival, not disease-specific survival. As such, we are unable attribute all deaths in the study to ACC. Due to the fact that adults likely have more co-morbidities and shorter life expectancies when compared to adults, the lack of disease-specific survival introduces the potential that differences in survival based on age may not be related to ACC in and of itself. Despite the limitations of this study, it represents the first study using a nationally representative sample to compare surgical outcomes and survival of ACC between pediatric and adult patients.
5. Conclusions
In this large, nationally representative cohort of patients, we compared surgical outcomes and survival between pediatric patients and adults presenting with adrenocortical carcinoma. We found that although there was no significant difference in baseline tumor characteristics, pediatric patients had improved overall survival at 1 and 5 years when compared to adult patients. Factors that were independently associated with worsened survival included increasing age, presence of other health comorbidities, presence of metastatic disease at presentation, and retroperitoneal lymph node resection. Future studies are needed to elucidate the potential role of adjuvant radiation therapy in pediatric patients with ACC. The study also highlights a need for evidence-based protocols that are based on disease stage in pediatric patients.
Funding
UNM was supported by the UNC Oncology Clinical Translational Research Training Program (K12CA120780).
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1.00
Overall survival by age group
Pediatric
Adult
Survival probabibility
0.75
I
0.50
NO
0.25
1
0.00
p=0.0016
0
12
24
36
48
60
72
84
96
108
120
Time from diagnosis (months)
| Pediatric (n = 71) | Adult (n = 2482) | |
|---|---|---|
| Age at Diagnosis, years | 3.0 (1.0-13.0) | 54.0 (43.0-65.0) |
| Sex | ||
| Female | 46 (64.8%) | 1502 (60.5%) |
| Male | 25 (35.2%) | 980 (39.5%) |
| White | 64 (90.1%) | 2146 (86.5%) |
| Hispanic | 13 (19.1%) | 160 (6.6%) |
| Primary Payor | ||
| Uninsured | 1 (1.4%) | 101 (4.1%) |
| Private Insurance | 37 (52.1%) | 1444 (58.2%) |
| Medicaid | 30(42.3%) | 173 (7.0%) |
| Medicare | 1 (1.4%) | 669 (27.0%) |
| Other Government | 1 (1.4%) | 44 (1.8%) |
| Insurance Status Unknown | 1 (1.4%) | 51 (2.1%) |
| Great Circle Distance, miles | 19.1 (9.1-36.2) | 14.9 (5.9-42.6) |
| Median Income Quartiles 2008-2012* | ||
| < $38,000 | 6 (9.1%) | 348 (15.2%) |
| $38,000-$47,999 | 13 (19.7%) | 533 (23.3%) |
| $48,000-$62,999 | 23 (34.9%) | 638 (27.8%) |
| ≥$63,000 | 24 (36.3%) | 773 (33.7%) |
| Health Status | ||
| Healthy | 65 (91.5%) | 1844 (74.3%) |
| Comorbidities | 6 (8.5%) | 638 (25.7%) |
| Tumor laterality | ||
| Right | 31 (43.7%) | 1104 (44.5%) |
| Left | 38 (53.5%) | 1337 (53.9%) |
| Tumor size | ||
| ≤5 cm | 6 (8.7%) | 323 (13.6%) |
| >5 cm | 63 (91.3%) | 2054 (86.4%) |
| Metastatic disease at diagnosis | ||
| No | 50 (74.6%) | 1841 (83.4%) |
| Yes | 17 (25.4%) | 366 (16.6%) |
| Pediatric (n = 71) | Adult (n = 2482) | p-value | |
|---|---|---|---|
| Adrenal surgery | 0.77 | ||
| Partial adrenalectomy | 15 (21.1%) | 536 (21.6%) | |
| Partial adrenalectomy | 15 (21.1%) | 536 (21.6%) | |
| Debulking | 0 (0.0%) | 36 (1.5%) | |
| Radical resection | 12 (16.9%) | 436 (17.6%) | |
| Receipt of regional lymph node surgery | <0.001 | ||
| No | 39 (54.9%) | 1883 (75.9%) | |
| Yes | 31 (43.7%) | 559 (22.5%) | |
| Chemotherapy | 0.023 | ||
| No | 35 (49.3%) | 1507 (62.6%) | |
| Yes | 36 (50.7%) | 901 (37.4%) | |
| External beam radiation | 0.040 | ||
| No | 77 (92.8%) | 2922 (84.5%) | |
| Yes | 6 (7.2%) | 534 (15.5%) | |
| Margin status | 0.99 | ||
| Negative | 46 (78.0%) | 1701 (78.1%) | |
| Positive | 13 (22.0%) | 478 (21.9%) | |
| Hospital length of stay, days | 64-9 | 53-7 | 0.011 |
| 30-day readmission | 11 (15.7%) | 158 (6.5%) | 0.003 |
| 30-day mortality | 0 (0.0%) | 60 (2.4%) | 0.18 |
| 90-day mortality | 2 (2.8%) | 139 (5.6%) | 0.31 |
| Follow up (months) | 53.0 (23.5-112.4) | 32.6 (13.6-66.8) | <0.001 |
| Characteristic | Survival at 1 year (%) (95% Confidence Interval) | Survival at 5 years (%)) | p-value (95% Confidence Interval) |
|---|---|---|---|
| Age | 0.0016 | ||
| <18 | 91. (81.2-96.0) | 60.6 (47.5-71.3) | |
| ≥18 | 79.6 (77.9-81.1) | 44.9 (42.7-47.0) | |
| Hispanic | 0.44 | ||
| No | 80.2 (78.5-81.8) | 45.6 (43.4-47.8) | |
| Yes | 76.8 (69.3-82.7) | 45.0 (36.3-53.3) | |
| Healthy | <0.001 | ||
| Yes | 82.3 (80.5-83.9) | 48.4 (46.0-50.8) | |
| No | 72.8 (69.2-76.1) | 36.1 (32.1-40.1) | |
| Metastatic disease at diagnosis | <0.001 | ||
| No | 85.1 (83.5-86.7) | 52.2 (50.0-54.6) | |
| Yes | 54.8 (49.7-59.7) | 12.4 (9.1-16.3) | |
| Receipt of lymph node surgery | |||
| No | 81.0 (79.2-82.7) | 47.3 (44.9-49.7) | |
| Yes | 76.8 (73.2-80.0) | 40.0 (35.7-44.2) | |
| Receipt of chemotherapy | 0.0019 | ||
| No | 79.2 (77.1-81.2) | 49.1 (46.4-51.7) | |
| Yes | 80.6 (77.9-83.0) | 38.2 (34.8-41.6) | |
| Receipt of external beam radiation therapy | 0.49 | ||
| No | 78.7 (76.9-80.5) | 44.9 (42.6-47.2) | |
| Yes | 44.9 (42.6-47.2) | 44.1 (38.7-49.3) |
| Characteristic | Hazard Ratio |
|---|---|
| Age ≥18 | 2.21 (1.50-3.27) |
| Private Insurance | 0.74(0.66-0.82) |
| Healthy | 0.69(0.61-0.78) |
| Metastatic disease at diagnosis | 3.51 (3.04-4.04) |
| Receipt of Lymph node surgery | 1.30 (1.14-1.48) |
| Receipt of chemotherapy | 0.94 (0.83-1.07) |
| Receipt of radiation therapy | 0.98 (0.84-1.15) |
| Characteristic | Hazard Ratio |
|---|---|
| Age ≥5 | 2.98 (0.87-10.2) |
| Private Insurance | 1.16 (0.42-3.19) |
| Healthy | 1.92 (0.45-8.22) |
| Metastatic disease at diagnosis | 3.02 (1.23-7.43) |
| Receipt of Lymph node surgery | 1.41 (0.59-3.37) |
| Receipt of chemotherapy | 2.26 (0.77-6.59) |
| Receipt of radiation therapy | 3.55 (0.92-13.7) |