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Published in final edited form as:

J Surg Res. 2018 December ; 232: 383–388. doi:10.1016/j.jss.2018.06.012.

A Phase II Trial of Cytoreduction and Hyperthermic

Intraperitoneal Chemotherapy for Recurrent Adrenocortical
Carcinoma
Marybeth S. Hughes, MDa, Winifred M. Lo, MDb, Tatiana Beresnev, MDb, Maria Merino, MDc,
Yvonne Shutack, MDb, R. Taylor Ripley, MDb, Jonathan M. Hernandez, MDb, Jeremy L.
Davis, MDb,*
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aDepartment of Surgery, Eastern Virginia Medical School, Norfolk, Virginia bThoracic and
Gastrointestinal Oncology Branch, National Cancer Institute, Bethesda, Maryland cTranslational
Surgical Pathology Section, National Cancer Institute, Bethesda, Maryland

Abstract
Background: Recurrent adrenocortical carcinoma (ACC) is an aggressive disease with few
options offering durable survival benefit. Despite metastasectomy, recurrence is common.
Cytoreduction and intraperitoneal chemotherapy have offered improved survival in other advanced
cancers. We sought to evaluate the use of cytoreduction and hyperthermic intraperitoneal
chemotherapy (HIPEC) for the treatment of recurrent intraperitoneal ACC.
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Methods: A phase II, single institution clinical trial was approved for patients with radiographic
evidence of resectable ACC limited to the peritoneum. Patients underwent treatment if optimal
cytoreduction was deemed possible at exploratory laparotomy. Primary outcome was
intraperitoneal progression-free survival. Secondary outcomes were treatment-related morbidities
and overall survival.

Results: Sixty-three patients were evaluated, of whom 11 met eligibility criteria. Nine patients
underwent cytoreduction and HIPEC, including one patient who recurred and was re-treated (n =
10 treatments). One patient could not be optimally cytoreduced for HIPEC and therefore did not
receive intraperitoneal chemotherapy. There was no perioperative mortality; perioperative
comorbidities were limited to Clavien-Dindo grade 2 or 3 and included hematologic, infectious,
and neurologic complications.
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Seven patients experienced disease recurrence and two patients died of disease during follow-up
(median 24 mo). Intraperitoneal progression-free survival was 19 mo, and median overall survival
has not yet been reached.

*
Corresponding author. Center for Cancer Research, National Cancer Institute, National Institutes of Health, Building 10, Room
4-3742, Bethesda, MD 20892. Tel.: +301 496 2126; fax: +301 451 6933., jeremy.davis@nih.gov (J.L. Davis).
Authors’ contributions: M.S.H. contributed for trial design and coordination; T.B., Y.S. contributed to trial coordination and patient
care; M.S.H., W.M.L., R.T.R., J.L.D., M.M. contributed to patient care; M.S.H., W.M.L., J.M.H., J.L.D. contributed to data analysis
and manuscript writing.
Disclosure
The authors reported no proprietary or commercial interest in any product mentioned or concept discussed in this article.
 Hughes et al. Page 2

Conclusions: Cytoreduction and HIPEC can be performed safely in selected patients. Patients
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with recurrent ACC confined to the peritoneal cavity can be considered for regional therapy in
experienced hands. However, disease recurrence is common, and other treatment options should be
explored.

Keywords
Adrenocortical carcinoma; Cytoreduction; Intraperitoneal chemotherapy

Introduction
Adrenocortical carcinoma (ACC) is a rare tumor with an estimated 5-y survival of 25%–
35%.1,2 Despite complete surgical resection, disease recurrence is observed in up to 85% of
patients.2,3 Systemic chemotherapy (e.g., etoposide, doxorubicin, cisplatin, and mitotane)
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offers modest benefit in progression-free survival (PFS) but no benefit in overall survival.1,4
Targeted molecular therapy with tyrosine kinase (i.e., imatinib, sunitinib), angiogenesis (i.e.,
bevacizumab), and mTOR (i.e., everolimus) inhibitors also provide no demonstrable survival
benefit.5 Metastasectomy for recurrent and/or metastatic ACC has been reported previously
as safe and associated with improved PFS and overall survival. However, evidence suggests
that recurrence is common after metastasectomy.6–11

Cytoreductive surgery (CRS) with hyperthermic intraperitoneal chemotherapy (HIPEC) is a

treatment strategy that achieves locoregional disease control and has been associated with
improved survival in advanced malignancies like appendiceal, colorectal, and ovarian
cancers.12 CRS with HIPEC allows direct contact of chemotherapy with tumor cells at a
higher concentration than would be tolerated with systemic administration. The combination
of chemotherapy and hyperthermia may have a synergistic, toxic effect on residual
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microscopic tissue remaining after resection, thus improving local control. Given the
ineffectiveness of systemic chemotherapy for recurrent ACC, alternative treatment strategies
warrant consideration. The aim of this study was to evaluate the impact of CRS and HIPEC
on intraperitoneal PFS (IP-PFS), treatment-related morbidity, and overall survival in patients
with recurrent and/or metastatic ACC limited to the peritoneal cavity.

Methods
Patient and study design
This single-institution, phase II clinical trial received approval from the institutional review
board. Informed consent was obtained prior to treatment according to protocol (Clinical-
Trials.gov identifier: NCT01833832) by a single surgeon (M.S.H.). Enrollment took place
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from April 2013 to September 2016, and all patients were treated at the Clinical Research
Center at the National Institutes of Health. All patients had histologic confirmation of ACC
with disease confined to the peritoneal compartment by cross-sectional imaging. Patients
with limited pulmonary metastases were eligible if deemed completely resectable by a
thoracic surgeon. All intraperitoneal diseases were amenable to resection or ablation
according to cross-sectional imaging in the absence of massive ascites or intestinal
obstruction. Patients were aged ≥18 y, Eastern Cooperative Oncology Group performance

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status 2 or less, and life expectancy greater than 3 mo. Patients were excluded from
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participation if they had a history of congestive heart failure, an ejection fraction less than
40%, creatinine greater than 1.5 mg/dL, significant chronic obstructive pulmonary disease,
cirrhosis, peripheral neuropathy of grade 2 or greater, brain metastases, pregnancy or active
breastfeeding status, history or evidence of severe portal hypertension, or evidence of active
systemic infection.

All patients underwent a thorough preoperative evaluation, including medical history,

physical examination, routine laboratory studies, baseline echocardiogram (in the instance of
prior doxorubicin treatment), and computed tomography imaging of the chest, abdomen, and
pelvis. Magnetic resonance imaging brain, positron emission tomography-computed
tomography, and magnetic resonance imaging liver were obtained only as clinically
indicated. Histologic diagnosis of ACC was independently confirmed by two pathologists.
The modified Weiss criteria were utilized for diagnosis of ACC.13 At operation, exploratory
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laparotomy was performed, and patients were assessed for extent of disease. Residual
disease was classified by completeness of cytoreduction k (CCR): CCR 0, no gross residual
disease; CCR 1, fewer than 100 total lesions, all smaller than 5 mm; CCR 2, more than 100
total lesions all less than 5 mm or any one lesion greater than 5 mm; and CCR 3, residual
tumor larger than 1 cm.9 HIPEC was performed for patients successfully reduced to CCR 0
or 1. HIPEC was performed using the closed-abdomen technique. Cisplatin (250 mg/m2-L
of perfusate) was circulated at approximately 1.0 L/min, with target intra-abdominal
temperature of 40◦C for 90 min. During perfusion, constant manual agitation of the
abdomen was performed to enable even distribution of the perfusate. Patients also received
intravenous sodium thiosulfate upon perfusion (loading dose 7.5 g/m2, then subsequent
maintenance infusion of 2.13 g/m2) and for a total of 12 h after initiation for renal protection
and limitation of cisplatin toxicity.14,15
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Endpoints and assessments

The primary endpoint was IP-PFS as measured from date of cytoreduction and HIPEC.
Progressive disease was defined as radiographic evidence of new lesions or ascites.
Secondary endpoints included treatment-related morbidity and overall survival.

Assessment methods included postoperative evaluation at 4–8 wk after operation and as

clinically indicated until recovery to baseline. Formal evaluations with physical exam,
laboratory assessment, and cross-sectional imaging were performed every 3 mo for the first
year, every 4 mo for the second year, and every 6 mo for every year thereafter until disease
progression or death. Ateach clinic visit, patients were assessed for treatment toxicity,
adverse events, quality of life (QoL), and disease progression by imaging and tumor markers
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where applicable. Complications were assessed by the Clavien-Dindo classification.

QoL characteristics were collected using the FACT-G questionnaire (version 4, http://
www.facit.org/facitorg/questionnaires), a validated survey that interrogates physical,
emotional, functional, and social well-being in cancer-related issues on a 5-point scale.
Potential scores range from 0 to 108 points, with higher scores corresponding to better QoL.
QoL was assessed prior to surgery, 6 wk postsurgery, and in regular intervals at 3, 6, 9, and
12 mo after the operation.

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Statistics
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Historical data indicate that patients with advanced ACC experience a median PFS of 5 mo.
It was estimated that the combination of CRS and HIPEC may be associated with a median
PFS of 10 mo. Using a one-tailed, α = 0.10, it was estimated that 24 patients would be
required to have 80% power to determine a 5-mo improvement in PFS.16

Results
Patients
Sixty-three patients with advanced ACC were evaluated for eligibility, of whom 53 did not
meet inclusion criteria. Eleven patients were eligible for study enrollment and were
scheduled for operation (Fig. 1), including one patient who was re-enrolled and re-treated
with a second CRS and HIPEC procedure after a local recurrence following the initial
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operation. At operation, one patient was deemed ineligible because optimal cytoreduction
could not be achieved, resulting in a total of 11 operations and 10 treatments with HIPEC.
At exploration, median peritoneal cancer index was 8 (range 3–16). Demographics of the
patients included in the analysis are detailed in Table 1.

Safety
Median operative time was 667 min (range 577–894 min) and was associated with median
estimated blood loss 500 mL (range 150–2000 mL); no patients required reoperation (Table
2). Monitored care in intensive care unit was brief (median 2 d, range 2–4) and length of stay
was less than 2 wk (median 10 d, range 8–13). There were no perioperative mortalities.
Complications were all Clavien-Dindo grade 2 or 3. These included infectious complications
(urinary tract infection, subcutaneous abscess), hematologic complications (anemia,
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thrombocytopenia), and neurologic complications (abdominal pain).

QoL and survival

Data on QoL were available for all patients through 3 mo after surgery. Mean FACT-G score
prior to intervention was 82.6. At 6 wk, mean FACT-G score had trended to 76.4 but
recovered to 80.2 by 3 mo after surgery. Social well-being remained stable throughout
follow-up. Functional well-being decreased (mean score 19 from 21, preoperatively),
whereas emotional well-being increased (mean score 17 from 13, preoperatively) (Fig. 2).

At time of data analysis, median follow-up was 23 mo. Median IP-PFS was 19 mo (range 3–
66 mo, Fig. 3). Seventy percent of treated patients experienced recurrent disease. Median
overall survival has not yet been reached. At time of analysis, three patients had died due to
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disease. Univariate and multivariate analyses were not performed given the small sample
size.

Discussion
The current clinical trial examined the feasibility, safety, and efficacy of CRS with HIPEC in
attaining local-regional tumor control for patients with local-regional recurrence of ACC.
Cytoreduction and HIPEC was proposed to offer the benefit of tumor debulking with

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additional disease control via regional administration of chemotherapy, potentially

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enhancing the durability of recurrence-free survival afforded by cytoreduction alone.

Although our study failed to meet target accrual, we believe the results of our trial add a
potential tool to the multidisciplinary armamentarium for clinicians who often have no
viable treatment to offer. It is possible that this strategy, in conjunction with serial
metastasectomy, could result in prolonged survival for patients until more efficacious
systemic therapy can be demonstrated.

Cytoreduction and HIPEC have been described in treatment of peritoneal metastasis due to
colorectal, ovarian, mesothelial, gastric, and appendiceal malignancies. It is well-established
that cytoreduction and HIPEC procedures have associated perioperative morbidities.
Reported rates of postoperative morbidity and mortality vary widely depending upon study,
with postoperative morbidity ranging from 12% to 62% and postoperative mortality ranging
from 0.9% to 7.7%.17–21 Common complications include wound infection, sepsis,
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respiratory failure, anastomotic leak, pneumonia, and enterocutaneous fistulae.18,21 In our

cohort, there was no perioperative mortality, and comorbidities were limited to moderate
grade infectious, hematologic, and other perioperative sequelae (i.e., hoarsensess after
intubation, abdominal pain). Therefore, cytoreduction and HIPEC appeared reasonably safe
and tolerable for selected patients with recurrent ACC.

Treatment by cytoreduction and HIPEC achieved median IP-PFS of 19 mo in this study. It is

challenging to compare this result with the heterogeneous outcome measures from the
paucity of studies reporting surgical management of locally advanced or recurrent ACC. A
study by Datrice et al.9 examined 57 patients with metastatic or recurrent ACC who
underwent 116 procedures including 23 liver resections, 48 lung or thoracic resections, and
15 exploratory laparotomies for resection. Although detailed patient and treatment
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information were not available, the authors reported a median PFS of 6 mo in their cohort. In
contrast, studies assessing disease-free interval after hepatectomy for liver metastases have
reported median disease-free survival of 7 to 9.1 mo.8,22 Even though direct comparisons
cannot be made, our findings suggest that cytoreduction and HIPEC may potentially impart
longer IP-PFS when compared to metastasectomy alone.

Overall survival is the most meaningful outcome metric for evaluating patients with
recurrent or metastatic ACC. The FIRM-ACT trial demonstrated no difference in overall
survival between patients who were treated with streptozocinmitotane compared to
combination chemotherapy (etoposide, doxorubicin, cisplatin, mitotane; 12 versus 13.8 mo).
Prior surgical studies evaluating pulmonary metastasectomy for limited oligometastatic
disease have reported overall survival rates ranging from 27 to 50.2 mo.9–12,23 Median
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overall survival had not yet been reached at the time of this analysis (median length of
follow-up: 23 mo). While definitive conclusions regarding overall survival benefit from
cytoreduction and HIPEC cannot be made, it appears that this intervention may be combined
with systemic chemotherapy to offer improved survival. As such, cytoreduction and HIPEC
could be considered for highly selected patients as an alternative to current systemic therapy.

The study limitations are worth noting. Accrual to this study was suboptimal. Despite
evaluation of 63 patients for study eligibility, 53 were not eligible due to strict inclusion

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criteria (84%). Although our institution has served as a major referral center for patients
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with ACC, both the eligibility criteria and single-institution nature of the study likely
contributed to poor patient accrual. Limited treatment numbers also hindered our ability to
examine any patient or treatment factors associated with outcomes after cytoreduction and
HIPEC. However, these issues are common to any study of a rare disease, particularly one in
which surgical therapy is difficult to standardize.

This study demonstrates that patients can be treated safely with CRS and HIPEC and that
prolonged IP-PFS can be achieved in selected patients. The frequency of recurrent disease
and advanced stage at diagnosis make ACC particularly challenging to manage suggesting
that tumor biology supersedes aggressive local therapy and that improved treatment options
are desperately needed. Systemic therapy and metastasectomy may yield limited survival
benefit, but there remain few viable treatment alternatives for patients with recurrent or
advanced ACC. As such, novel treatment strategies for managing this disease merit
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exploration.

Acknowledgment
The authors gratefully acknowledge the clinical assistance of Tito Fojo, MD, PhD, Prakash Pandalai, MD, Udo
Rudloff, MD, and Dan Zlott, PharmD, and the guidance of Seth Steinberg PhD in the statistical aspects of the
protocol.

Funding:
This study was funded through the Intramural Research Program of the National Cancer Institute.

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23. Bellatone R, Ferrante A, Boscherini M, et al. Role of reoperation in recurrence of adrenal cortical
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Fig. 1 –.
Clinical trial design and enrollment. *1 patient experienced recurrent disease and was re-
enrolled for a second CRS and HIPEC procedure.
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Fig. 2 –.
FACT-G questionnaire QoL scores for cohort (median score shown).
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Fig. 3 –.
(A) Overall survival of cohort (median survival not yet reached). (B) IP-PFS (median
survival 19 mo).
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Table 1 –

Patient cohort demographics.

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Factor median (range) % Median (range) %

Age 41 (24–58)
Gender
Male 3 30
Female 7 70
Tumor stage (AJCC) at diagnosis
I 2 20
II 5 50
III 1 10
IV 0 0
unknown 2 20
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Functional tumor status

Non-functional 4 40
Functional 6 60
Type of resection
Open 4 40
Laparoscopic 4 40
Unknown 2 20
Prior resection margin
R0 7 78
R1 2 22
Unknown 1 10
DFI from initial resection (mo)
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<12 0 0
12–24 5 50
25+ 4 40

Unknown* 10 10

Prior treatment: mitotane

No 3 30
Yes 7 70
Prior treatment: EDP
No 8 80
Yes 2 22
Prior treatment: radiation or RFA
No 6 67
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Yes 4 40
Time between evidence of disease and HIPEC (y) 1.25
Comorbidities
CAD 0 0
COPD/asthma 1 10

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Factor median (range) % Median (range) %

CKD 0 0
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ECOG
0 10 111
1 0 0

CAD = coronary artery disease; CKD = chronic kidney disease; COPD = chronic obstructive pulmonary disease; DFI = disease free interval;
ECOG = Eastern Cooperative Oncology Group; EDP = etoposide, doxorubicin, cisplatin; HPI = history of present illness; RFA = radiofrequency
ablation.
*
Unclear from initial HPI, how long initial disease-free interval was.
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Table 2 –

Perioperative characteristics.
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Perioperative characteristics* Median Range/%

Sites of metastatic disease

Adrenal ed 2 18.2
Liver 3 27.3
Lung 2 18.2
Spleen 1 9.1
Retroperitoneal space 6 54.5
Diaphragm 2 18.2
Pelvis 1 9.1
Abdominal wall 1 9.1
Operative time (min) 645 (577–894)
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Peritoneal cancer index status

Before CRS 8 (3–16)
After CRS 0 (0–6)
CCR score 0 (0–2)
Estimated blood loss (mL) 500 (150–2000)
Transfusion
Packed red blood cells 2 (0–8)
Fresh frozen plasma 0 (0–5)
platelets 0 (0–6)
Length of ICU stay (d) 2 (2–4)
Length of hospital stay (d) 10 (8–13)
Perioperative mortality 0 0
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Perioperative morbidity
Cardiac events 0 0
Respiratory events 0 0
Acute kidney injury 0 0
Infection 3 30
Wound dehiscence 1 10

ICU = intensive care unit.

*
Based on n = 11 patient treatments, including one patient who underwent cytoreduction alone.
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