Case Reports in Oncology

Case Rep Oncol 2024;17:377-385

DOI: 10.1159/000535367

Received: August 22, 2023

Accepted: November 6, 2023

Published online: February 27, 2024

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This article is licensed under the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC) (http://www.karger.com/Services/OpenAccessLicense). Usage and distribution for commercial purposes requires written permission.

Case Report

Adrenocortical Carcinoma with a Renal Vein Thrombus Extending to the Inferior Vena Cava Successfully Resected with the Left Kidney and Distal Pancreatectomy: A Case Report

Takashi Miyata Yuta Sannomiya Taigo Nagayama Ryosuke Kin Hisashi Nishiki Akifumi Hashimoto Daisuke Kaida Hideto Fujita Nobuhiko Ueda Hiroyuki Takamura

Department of General and Digestive Surgery, Kanazawa Medical University Hospital, Ishikawa, Japan

Keywords

Adrenocortical carcinoma . Tumor thrombus . Inferior vena cava . Adjuvant therapy . Radiotherapy · Case report

Abstract

Introduction: Adrenocortical carcinoma (ACC) is an extremely rare and aggressive tumor, and its clinical characteristics are poorly defined because of its rarity. Case Presentation: We report a 64-year-old man who presented with upper abdominal pain and weight loss. Computed tomography revealed a 15 cm left adrenal tumor compressing the pancreas ventrally and a tumor thrombus in the inferior vena cava (IVC) originating from the left renal vein. Positron emission tomography-computed tomography revealed 18F-fluorodeoxyglucose uptake only in the tumor and tumor thrombus, and radical surgery was planned. Intraoperatively, the tumor was visible on the posterior stomach wall, and the tumor adhered to the pancreas and left kidney. We excised the tumor with part of the pancreas and the left kidney and excised the thrombus from the IVC after clamping. The final diagnosis was ACC, tumor-node-metastasis grade T3N1M0, stage III. The patient received chemotherapy and radiotherapy postoperatively; however, two liver metastases appeared 6 months after surgery. Chemotherapy was continued, and no exacerbation of the liver metastases was observed. Posterior segment resection of the liver was performed 16 months after the initial surgery. Conclusion: This report of a rare case of ACC involving the pancreas with tumor thrombus extension to the IVC stresses that this

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Case Reports in OncologyCase Rep Oncol 2024;17:377-385
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Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

combination of conditions does not preclude radical surgery. However, more data are needed regarding chemotherapy and radiotherapy, as well as relapse treatment, and further research on ACC is essential for a favorable prognosis.

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Introduction

Adrenocortical carcinoma (ACC) is an extremely rare tumor with an annual incidence of only 1-2 cases per million [1]. Non-functional tumors of hormonal tissues account for approximately 40% of ACC lesions, and owing to the lack of endocrine symptoms, a diagnosis can only be made when the tumor is large and causes symptoms, such as abdominal pain [2]. Therefore, non-functional ACC tumors often exceed 10 cm in size, with stage III or stage IV ACC accounting for approximately 80% of all such tumors. Moreover, the prognosis of ACC is poor, and the 5-year overall survival rate is 16-35% [3]. Therefore, the clinical features and therapeutic strategies of ACC remain unknown. In this study, we report a rare case of ACC with a renal vein thrombus extending to the inferior vena cava (IVC) that was resected with the left kidney and distal pancreatectomy in a man who was subsequently able to undergo hepatic resection for primary postoperative liver metastases.

Case Report

A 64-year-old man was admitted to our institution with a recent onset of upper ab- dominal pain and weight loss. His medical and family history was unremarkable, and he was not taking medications. The physical examination was unremarkable, with normal vital signs and a non-cushingoid appearance. Laboratory data revealed slight leukocytosis, whereas other data, namely, serum tumor markers and plasma-free metanephrines, aldosterone, potassium, and testosterone, were within their normal ranges (Table 1). Computed to- mography and magnetic resonance imaging revealed a 15 cm enhancing left adrenal mass compressing the pancreatic body ventrally (Fig. 1a). The tumor embolism continued to the IVC below the liver approximately 4-5 cm downstream from the left renal vein (Fig. 1b-d). Positron emission tomography illustrated that only the tumor and thrombus exhibited in- creased uptake of 18F-fluorodeoxyglucose, and there were no obvious distant metastases. No abnormal uptake in the tumor was seen on I-123 metaiodobenzylguanidine scintigraphy. The patient was diagnosed with left ACC with an IVC tumor thrombus. He underwent radical surgery after transcatheter arterial embolization (TAE) of the main supplying arteries of the tumor and IVC temporary filter placement 1 day before surgery.

The tumor was located on the posterior wall of the body of the stomach and the body of the pancreas (Fig. 2a), extending above the body of the stomach, on the right side of the aorta, and below the left renal vein. Because the tumor had adhered to the pancreatic body and left kidney, the pancreatic parenchyma was divided at the level of the root of the splenic artery (Fig. 2b). This was followed by mobilizing the left kidney, pancreatic tail, and spleen. We then taped the left renal vein, which was dilated by a tumor thrombus (Fig. 2c). The IVC upstream and downstream of the confluence of the left renal vein and right renal vein were clamped. Subsequently, the confluence of the left renal vein and IVC was opened, the tumor thrombus was successfully removed from the IVC with no adhesion observed in the IVC, and we divided

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Case Rep Oncol 2024;17:377-385

DOI: 10.1159/000535367

@ 2024 The Author(s). Published by S. Karger AG, Basel www.karger.com/cro

Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

Case Reports in Oncology

Table 1. Results of laboratory tests on admission
VariablesLaboratory tests results
WBC, ×103/uL12.25
RBC, ×106/HL488
Hemoglobin, g/dL15.5
Hematocrit, %45.3
Platelet, ×104/uL22.4
Total protein, g/dL6.5
Albumin, g/dL3.4
CRP, mg/dL0.15
BUN, mg/dL8
Creatinine, mg/dL0.95
Na, mEq/L142
K, mEq/L3.4
Cl, mEq/L106
AST, IU/L22
ALT, IU/L31
ALP, IU/L155
LDH, IU/L192
Total bilirubin, mg/dL0.4
Direct bilirubin, mg/dL0.2
Amylase, IU/L97
CK, U/L14
T-chol, mg/dL207
TG, mg/dL213
HDL-C, mg/dL45
LDL-C, mg/dL133
BS, mg/dL128
PT-INR1.08
PT, %87
APTT, s39.4
CEA, ng/ml1.7
CA19-9, U/mL19.3
CA125, U/mL12.3
Adrenaline, pg/mL11
Noradrenaline, pg/mL134
Dopamine, pg/mL8
ACTH, pg/mL10.1
Cortisol, µg/dL25.79
Renin, ng/ml/h0.6
Aldosterone, pg/mL144
Progesterone, ng/ml1.06

Case Reports in Oncology

Table 1 (continued)
Case Rep Oncol 2024;17:377-385
DOI: 10.1159/000535367@ 2024 The Author(s). Published by S. Karger AG, Basel www.karger.com/cro

Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

VariablesLaboratory tests results
Testosterone, ng/dL3.74
LH, mIU/mL2.0
FSH, mIU/mL0.7
Prolactin, ng/ml10.8

WBC, white blood cell; RBC, red blood cell; CRP, C-reactive protein; BUN, blood urea nitrogen; AST, aspartate aminotrans- ferase; ALT, alanine aminotransferase; ALP, alkaline phospha- tase; LDH, lactate dehydrogenase; CK, creatine kinase; T-chol, total cholesterol; TG, triglycerides; HDL-C, high-density lipo- protein cholesterol; LDL-C, low-density lipoprotein cholesterol; BS, blood sugar; PT-INR, prothrombin time-international nor- malized ratio; PT, prothrombin time; APTT, activated partial thromboplastin time; CEA, carcinoembryonic antigen; CA19-9, carbohydrate antigen 19-9; CA125, cancer antigen 125; PTH, parathyroid hormone; PTHrP, parathyroid hormone-related peptide; ACTH, adrenocorticotropic hormone; LH, luteinizing hormone; FSH, follicle stimulating hormone.

the left renal vein and removed the specimen en bloc (Fig. 2d-f). The IVC clamp time was 11 min, the operative time was 443 min, and the intraoperative blood loss was 3,480 mL.

The excised specimen weighed 1.2 kg (Fig. 3a), and histopathology confirmed the di- agnosis of ACC, T3N1M0, stage III (International Union Against Cancer, eighth edition). Immunohistochemically, the tumor was positive for anti-steroidogenic factor-1 antibody, its cells were positive for calretinin and inhibin a were positive, and approximately 38% of the cells were positive for Ki-67 (Fig. 3b-f). Postoperatively, the IVC filter was removed on postoperative day 2, and the patient developed a pancreatic fistula (Clavien-Dindo IIIa) and an intra-abdominal abscess (Clavien-Dindo IIIa), which were treated conservatively. The patient received mitotane as adjuvant chemotherapy on postoperative day 14, and he was discharged on postoperative day 50. Radiotherapy (54 Gy) was also administered as local treatment. Unfortunately, two liver metastases developed recurred 6 months after the operation (Fig. 4a). However, chemotherapy with etoposide, doxorubicin, and cisplatin was continued, and no new lesions or tumor progression were observed. Posterior segmentectomy was performed for the liver metastases 16 months after the first operation (Fig. 4b, c). Post- operatively, mitotane chemotherapy was continued, but peritoneal dissemination was ob- served 7 months after the second operation, and the patient requested palliative treatment. The patient subsequently died 4 months later due to the liver failure.

Discussion

ACC is a rare aggressive malignant tumor associated with a poor prognosis. ACC with tumor thrombus extension into the IVC is even rarer [1, 4]. ACC with an IVC thrombus was first reported by Castleman et al. [5], and the first case was found during surgery. However, there are few reports of ACC with an IVC tumor thrombus, and the postoperative course and utility of surgery must be examined in future studies.

The established treatment in patients with ACC remains to be clarified, although ag- gressive surgery is considered potentially curative [3]. Chiche et al. [4] reported 15 cases of

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Case Reports in Oncology

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Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

Fig. 1. Preoperative contrast-enhanced computed tomography (CT). a Enhanced abdominal CT revealing a 15 cm enhancing left adrenal mass compressing the pancreatic body ventrally. The red arrow denotes the splenic artery, and the yellow arrows denote the pancreatic body and tail compressed by the tumor. b, c CT revealing the tumor embolism continuing to the inferior vena cava (IVC) below the liver approximately 5 cm downstream from the left renal vein and left adrenal vein. The red arrow in b denotes the thrombus in the left renal vein. The red arrow in c denotes a thrombus in the IVC, and the yellow arrow in c denotes a thrombus in the left adrenal vein. d Magnetic resonance image revealing a 15 cm mass located in the left adrenal gland. The image also presents tumor thrombus extension into both the left renal vein and IVC.

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extended surgery for ACC with an IVC tumor thrombus. Six patients required a heart-lung machine, and 2 patients who experienced hypothermia or cardiac arrest and required heparin neutralization died of thrombosis associated with IVC replacement [4]. In 6 patients with ACC with an IVC tumor thrombus who underwent hepatectomy, two underwent lobectomy, and four underwent segmental resection, three of whom were positive for liver infiltration [6]. There were no postoperative deaths, but the 2 patients who underwent lobectomy experi- enced postoperative complications, such as severe liver failure [6]. Based on these findings, IVC replacement or hepatectomy has a high risk of serious postoperative complications, and although pancreatic resection was necessary in the present case, and the postoperative course was prolonged owing to the presence of a pancreatic fistula, the ability to remove the tumor without IVC replacement or hepatectomy was considered to contribute to a relatively good course.

Radical surgery for large ACC with an IVC thrombus is a major invasive surgery, and careful preoperative preparation is required. We performed IVC filter placement and em- bolization of feeding vessels as preoperative preparations. During surgery with tumor em- bolism in the IVC, released tumor fragments can cause pulmonary embolism. Additionally, tumor embolism caused by ACC has a high risk of pulmonary embolism because the thrombus is gelatinous and brittle [4]. Intraoperative pulmonary embolism is often fatal, and I think it is

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Case Reports in Oncology

Case Rep Oncol 2024;17:377-385

DOI: 10.1159/000535367

@ 2024 The Author(s). Published by S. Karger AG, Basel www.karger.com/cro

Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

Fig. 2. Intraoperative observation. The tumor was located in the posterior wall of the pancreatic tail ex- tending from the gastric cardia, and its diameter was approximately 15 cm. The yellow arrows in a are the pancreas. b The pancreatic parenchyma was divided at the level of the root of the splenic artery. c After distal pancreatic resection, splenectomy, and left nephrectomy, the left renal vein and inferior vena cava (IVC) were exposed and taped with the left renal vein with the intravascular tumor embolism. d Blood circulation was blocked after taping the IVC in the lower part of the liver, the right renal vein, and the IVC downstream from the right renal vein. e The IVC was incised on the side at the base of the left renal vein, and the tumor thrombus was removed. f Photograph after tumor removal.

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necessary to actively use IVC filters in cases like this one where there is a high possibility of intraoperative pulmonary embolism [7]. However, there are few reports of its use in the treatment of ACC with IVC thrombus, so further research is needed [8]. Additionally, in- traoperative transesophageal echocardiography has been reported to be effective in diag- nosing pulmonary embolism, and although we did not perform it, it should have been considered [8]. Performing preoperative TAE for tumors in other organs is expected to reduce the amount of intraoperative bleeding [9]. To our knowledge, there are no reports of pre- operative TAE for adrenal tumors, and in our case, the amount of bleeding required blood transfusion even after TAE. However, if a large amount of bleeding is expected by preoperative examination, preoperative TAE could represent an effective treatment, and as with IVC filters, further research is required.

Mitotane- or cisplatin-based chemotherapy is recommended as systemic treatment for ACC [10]. However, adjuvant therapy for ACC is controversial because of the limited number of randomized controlled trials owing to the low incidence of the disease [11]. Recently, the European Society of Endocrinology and ENSAT 2018 guidelines recommend adjuvant mi- totane treatment in more than 10% of patients with ACC who are positive for Ki-67, but further case numbers and examination including use of cytotoxic agents are necessary over the world [12]. There are several reports of postoperative local radiotherapy showing mixed results. One report found that adjuvant radiotherapy had a significant effect on local

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Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

Fig. 3. a Macroscopic findings of the resected specimens revealing a relatively soft yellow tumor. The yellow arrow denotes the pancreatic dissection stump, and the red arrow denotes the left renal vein tumor thrombus. b Pathological findings of the tumor cells with a high nucleus-to-cytoplasmic ratio, acidophilic to clear polygonal cytoplasm, and irregular nuclei of various sizes, which are proliferating solidly (original magnification, ×100; hematoxylin and eosin stain). Tumor cells stained positively for steroidogenic factor-1 antibody (c), calretinin (d), and inhibin a (e). f The Ki-67 labeling index was 38% (c-f, original magnification, ×100).

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recurrence but had no effect on disease survival and OS [13], while other reports were found to be associated not only with local recurrence but also with improved OS [14]. However, there are still no prospective data to confirm the value of adjuvant radiotherapy, and the results of retrospective data should be interpreted with caution due to potential referral and selection bias.

The most common metastatic sites in postoperative ACC recurrence are the lungs, liver, and local sites. Metastatic and recurrent ACC carries poor 5-year survival rates of lower than 15%, and the optimal management for recurrent ACC is currently unclear [1]. In our case, hepatectomy was performed for recurrent liver metastasis, but distant metastasis recurrence was subsequently observed. However, there are also reports in which liver metastasis was resected and long-term results were obtained, albeit in small cohorts [12]. It is necessary to accumulate cases and further consider the timing of chemotherapy and surgery while considering resection.

In conclusion, we propose that extension of the tumor thrombus into the IVC and invasion into the pancreas alone should not be considered a contraindication for radical surgery in patients with ACC, and radical surgery is considered indispensable. However, surgery alone might be insufficient, and because this is a rare disease, further evaluation of chemotherapy and radiotherapy, as well as surgical treatment after recurrence, is necessary. We believe that this report will be useful in the future clinical diagnosis and treatment of this disease. The

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Case Reports in Oncology

DOI: 10.1159/000535367

Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

Fig. 4. Postoperative contrast-enhanced computed tomography. a Two liver metastases were observed 6 months after the operation (red arrows). b Photograph after liver removal. c Macroscopic findings of the resected specimens.

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CARE Checklist has been completed by the authors for this case report, attached as online supplementary material (for all online suppl. material, see https://doi.org/10.1159/ 000535367).

Acknowledgment

We thank Joe Barber Jr., PhD, from Edanz (www.edanz.com/ac) for editing a draft of this manuscript.

Statement of Ethics

Ethical approval is not required for this study in accordance with local or national guidelines. Written informed consent was obtained from the patient’s next of kin for pub- lication of the details of their medical case and any accompanying images.

Conflict of Interest Statement

The authors declare that they have no competing interests.

Funding Sources

No authors received any funding for this paper.

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Case Rep Oncol 2024;17:377-385

DOI: 10.1159/000535367

@ 2024 The Author(s). Published by S. Karger AG, Basel www.karger.com/cro

Miyata et al .: Adrenocortical Carcinoma with an Inferior Vena Cava Tumor Thrombus

Case Reports in Oncology

Author Contributions

T. Miyata and H.T. performed the surgery and held responsibility for the patient’s perioperative management. T. Miyata drafted the manuscript. Y.S., T.N., R.K., H.N., A.H., D.K., H.F., and N.U. also managed the patient. All authors have approved the manuscript.

Data Availability Statement

All data generated or analyzed during this study are included in this article and its online supplementary material. Further inquiries can be directed to the corresponding author.

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