Perfusion
Inferior vena cava tumor thrombus: clinical outcomes at a canadian tertiary center
Ali Fatehi Hassanabad,’ Chad G Ball2 and William T Kidd’
Perfusion 2024, Vol. 39(8) 1577-1586 C The Author(s) 2023
BY NG
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Abstract
Objective: This study reports the surgical management and outcomes of patients with malignancies affecting the IVC. Methods: This was a retrospective study that considered patients undergoing surgery for IVC thrombectomy in Calgary, Canada, from 1 January 2010 to 31 December 2021. Parameters of interest included primary malignancy, the extent of IVC involvement, surgical strategy, and medium-term outcomes.
Results: Six patients underwent surgical intervention for malignancies that affected the IVC. One patient had a retro- peritoneal leiomyosarcoma, 1 had hepatocellular carcinoma with thrombus extending into the IVC and right atrium, 1 had adrenocortical carcinoma with IVC thrombus extending into the right atrium, and 3 had clear cell renal cell carcinoma with thrombus extending into the IVC. Surgical strategy for the IVC thrombectomy varied where 5 patients required the institution of cardiopulmonary bypass and underwent deep hypothermic circulatory arrest. No patient died perioper- atively. One patient died 15-months post-operatively from aggressive malignancy.
Conclusion: Different types of malignancy can affect the IVC and surgical intervention is usually indicated for these patients. Herein, we have reported the outcomes of IVC thrombectomy at our center.
Keywords
IVC thrombus, surgical thrombectomy, deep hypothermic circulatory arrest, surgical outcomes
Introduction
Tumors involving the inferior vena cava (IVC) are either leiomyosarcomas, which arise directly from the vessel wall, or malignancies of other origins, which have invaded the IVC by direct endovascular extension and/or intraluminal thrombotic embolization.1 Primary leiomyosarcomas of the IVC are very rare, with only approximately 300 cases reported.2 Malignant tumors invading the IVC arise mostly from the retroperitoneal tissue, the kidneys, the suprarenal glands, the liver, testicles, ovaries, or the lungs.3.4 Indeed, renal cell cancer (RCC) is often associated with IVC invasion in 4%-10% of all patients,5 while in- volvement of the right atrium (RA) is encountered in 5%- 15%.º Conservative management of IVC tumors consist of chemotherapy and/or radiotherapy, but neither has proven to consistently improve long-term survival.7 Thus, in cases where malignant tumors invade the IVC, surgical intervention offers the most important positive prognostic factor for long-term survival and is considered the best treatment strategy. 8-10
Surgical treatment including complete or partial resection of the IVC should be considered even in
cases of advanced cancer. However, resection of tu- mors invading the IVC is challenging, and may require cardiopulmonary bypass (CPB), with or without deep hypothermic circulatory arrest (DHCA). This is es- pecially the case when there is an intracardiac tumor component, where CPB and DHCA are indicated to improve the safety and the efficacy of the surgical procedure, and to achieve a complete resection. 11-14 Whereas the perioperative complications of IVC re- section for leiomyosarcomas have been well de- scribed,2 the benefit of secondary IVC tumor resection remains unclear. Moreover, the surgical approach to
“Section of Cardiac Surgery, Department of Cardiac Sciences, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine, Calgary, Alberta, Canada
2Department of Surgery, Foothills Medical Center, Cumming School of Medicine, Calgary, Alberta, Canada
Corresponding author:
Ali Fatehi Hassanabad, Section of Cardiac Surgery Department of Cardiac Sciences, Libin Cardiovascular Institute Cumming School of Medicine Calgary, Alberta Canada.
Email: ali.fatehihassanabad@ahs.ca
the resection of tumors involving the retrohepatic portion of the IVC, the right heart chambers and/or the pulmonary arteries (PA) is not standardized. Supplementary Table S1 summarizes all of the clinical studies that have reported the surgical outcomes of IVC thrombectomy in adults. These studies, which exclude case reports, have been identified after an extensive search of the literature was performed (search algorithm and search results are provided in the Supplementary Material). The aim of this single- center, retrospective study of six patients is to describe our surgical approach to the resection of malignant tumors involving the IVC, and to report our outcomes.
| Age (mean ± SD) | 60.5 ± 9.7 |
|---|---|
| Gender Female | 0 |
| Male | 6 |
| Hypertension | 2 |
| Diabetes | 2 |
| Dyslipidemia | 2 |
| Smoking history | 2 |
| Coronary artery disease | 1 |
| Atrial fibrillation | 0 |
| Renal disease | 0 |
| Lung disease | 0 |
| Peripheral arterial disease | 0 |
| Cerebral vascular disease | 1 |
| Cerebrovascular event | 1 |
| Gastrointestinal disease | 3 |
| Pulmonary hypertension | 0 |
| Prior cardiac surgeries or procedures | 0 |
| ECOG status greater than 0 | 0 |
Abbreviations: ECOG: Eastern Cooperative Oncology Group; SD: Standard Deviation.
Methods
This is a retrospective study that considered a series of patients who presented with a malignancy that affected the IVC and required surgical IVC thrombectomy in Calgary, Canada. A chart review was conducted to re- trieve information on type of malignancy, extent and nature of IVC involvement, surgical strategy, and op- erative outcomes. Charts were reviewed from 1 January 2010 to 31 December 2021, and six patients were identified to have undergone surgical IVC thrombec- tomy. In addition to reporting the perioperative pre- sentation and details, clinical outcomes data at latest follow-up was also retrieved to enrich the literature with the short and intermediate surgical outcomes of IVC thrombectomy.
Case series
Herein, we present the details of the six patients that were identified to have undergone surgical intervention. Table 1 summarizes the baseline demographics for these patients including the Eastern Cooperative Oncology Group (ECOG) status at the time of index hospitali- zation. In Table 2, we present the malignancy and extent of IVC involvement in each patient, while Table 3 contains intraoperative information. Finally, Table 4 summarizes the clinical outcomes for each patient at 30-days post-surgery and latest follow-up.
Patient 1: retroperitoneal leiomyosarcoma
A 58-year-old male who was incidentally noted to have a nodule on his left adrenal 4 years prior to his presen- tation. Although he was asymptomatic during this pe- riod, he did have follow-up imaging after 1 year, which revealed an unchanged mass on his left adrenal and a new periadrenal mass on the right side. After 3 years without any symptoms, he presented with nausea,
| Primary malignancy and stage | Extent of IVC involvement |
|---|---|
| Patient 1: Retroperitoneal leiomyosarcoma; pT2b PNY | Right-sided retrocaval nodule with mass effect on the IVC and the presence of an IVC thrombus |
| Patient 2: Renal cell carcinoma (RCC); pT3cN1 | Clot present in the IVC and extending into the thoracic IVC (2.5 cm below the right atrium (RA) |
| Patient 3: Adrenocortical carcinoma; pT3N0 | IVC thrombus extending into the RA |
| Patient 4: Clear cell RCC; pT3a pNX | IVC thrombus extending into the RA |
| Patient 5: RCC; pT3bpN0pM1 Patient 6: Hepatocellular carcinoma (HCC); not staged | Thrombus extending into the IVC and the RA Thrombus extending into the intra-thoracic IVC and the gonadal vein |
Abbreviations: IVC: Inferior Vena Cava; HCC: Hepatocellular Carcinoma; RA: Right Atrium; RCC: Renal Cell Carcinoma.
| Patient | Intraoperative details |
|---|---|
| Patient 1: Retroperitoneal leiomyosarcoma | Cardiopulmonary bypass (CPB) time: 180 min |
| Mild hypothermic circulatory arrest (MHCA) Temperature: 28℃ | |
| Mild hypothermic circulatory arrest (MHCA) Duration: 30 min Blood product transfusions (units) | |
| 2 Packed red blood cells (pRBCs) | |
| 1 Platelets (plt) | |
| 1 Fresh frozen plasma (FFP) | |
| Patient 2: Renal cell carcinoma (RCC) | CPB time: 200 min |
| Deep hypothermic circulatory arrest (DHCA) Temperature: 16.5℃ | |
| Deep hypothermic circulatory arrest (DHCA) Duration: 26 min | |
| Blood product transfusions (units) | |
| 4 pRBCs | |
| 1 Plts | |
| 1 FFP | |
| Patient 3: Adrenocortical carcinoma | CPB time: 200 min |
| DHCA temperature: 17℃ | |
| DHCA duration: 20 min | |
| Blood product transfusions (units) | |
| 5 pRBCs | |
| 2 Plts | |
| 2 FFP | |
| 1 Cryopercipitate (CPP) | |
| 2 Fibrinogen | |
| 1 Albumin (5%) | |
| Patient 4: RCC | CPB time: 192 min |
| DHCA temperature: 17.5°℃ | |
| DHCA duration: 9 min | |
| Blood product transfusions (units) | |
| 3 pRBCs | |
| 1 Plts | |
| 1 FFP | |
| 1 Fibrinogen | |
| 2 Albumin (5%) | |
| Patient 5: RCC | No circulatory arrest required |
| Blood product transfusions (units) | |
| 2 pRBCs | |
| 1 FFP | |
| Patient 6: Hepatocellular carcinoma (HCC) | CPB time: 153 min |
| DHCA temperature: 16℃ | |
| DHCA duration: 5 min | |
| Blood product transfusions (units) | |
| 8 pRBCs | |
| 3 Plts | |
| 4 FFP | |
| 2 Fibrinogen |
Abbreviations: CPB: Cardiopulmonary Bypass; CPP: Cryoprecipitate; DHCA: Deep Hypothermic Circulatory Arrest; FPP: Fresh Frozen Plasma; HCC: Hepatocellular Carcinoma; MHCA: Mild Hypothermic Circulatory Arrest; Plts: Platelets; pRBCs: packed Red Blood Cells; RCC: Renal Cell Carcinoma.
fevers, headaches, and lower back pain. An abdominal CT showed a right-sided retrocaval nodule measuring 6.9 × 4.3 cm2 (Figure 1(a)). The nodule exhibited mass effect on the IVC with IVC thrombus (Figure 1(b)). Note was made of it abutting the medial right kidney. Further workup included a chest CT that showed multiple small pulmonary nodules. He was diagnosed
with retroperitoneal leiomyosarcoma (T2bN0M0) and underwent 28 rounds of neoadjuvant radiotherapy.
Surgical approach involved a midline laparotomy and a full median sternotomy. The patient’s liver was mobilized and rotated medially, while the duodenum was kocherized. A hard mass encasing the kidney and the lateral wall of the intrahepatic infrarenal IVC was
| Patient 1 | Patient 2 | Patient 3 | Patient 4 | Patient 5 | Patient 6 | |
|---|---|---|---|---|---|---|
| Blood product | None | 1 pRBCs | 1 pRBCs | I pRBCS | 1 pRBCs | None |
| transfusion in the | Plts | 1 Plts | ||||
| ICU | Albumin | 1 FFP | ||||
| 3 Albumin | ||||||
| Reoperation for bleeding | No | No | No | No | No | Yes |
| 30-days mortality | No | No | No | No | No | No |
| Cerebrovascular | No | No | No | No | No | Yes |
| event | ||||||
| Myocardial | No | No | No | No | No | No |
| infarction | ||||||
| Length of hospital stay (days) | 22 | 8 | 12 | 12 | 9 | 17 |
| Clinical status at latest follow-up | Asymptomatic and disease- free at 55 months | Asymptomatic and disease- free at | Died at 15 months | Asymptomatic and disease- free at | Asymptomatic and disease- free at | Asymptomatic and disease- free at 5 months |
| 48 months | 34 months | 18 months |
Abbreviations: FPP: Fresh Frozen Plasma; ICU: Intensive Care Unit; Plts: Platelets; pRBCs: packed Red Blood Cells; RCC: Renal Cell Carcinoma.
Fig 1A
Fig 1B
identified. The patient’s kidney was mobilized en- block to locate the posterior aspect of the IVC. The left renal artery and vein were then isolated and en- circled with a Vesseloop. At this point the patient was placed on CPB. Subsequently, mild hypothermic circulatory arrest was established at 28°. The in- frarenal IVC was then clamped below the tumor and the intrahepatic IVC was clamped above the tumor. The proximal IVC was divided below the tumor. Lumbar venous branches were clipped, and a LigaSure (Medtronic, CA, USA) cautery was used to mobilize the IVC en bloc with the tumor away from the ret- roperitoneal tissues. The right renal artery was divided
and clipped, while the left renal vein was divided as it entered the IVC. At this stage, the tumor was mo- bilized and resected at the distal aspect and normal IVC.
A 20 mm Gore-Tex (Gor-Tex Vascular Grafts, AZ, USA) tube graft was then used at the infrahepatic IVC, followed by deairing and removal of clamps. While the patient was being rewarmed, the graft was re-clamped and another portion of the 20 mm Gore-Tex graft was used to implant the left renal vein in a side to side fashion. Patient was weaned from CPB, and protamine was administered. On 4-years follow-up the patient is symptom-free and living at home.
Patient 2: Renal cell carcinoma (RCC) with extension into the juxtarenal, retrohepatic, and thoracic IVC
An otherwise healthy 47-year-old male who presented with 1-month of progressively worsening dyspnea and fatigue. A CT scan revealed a 10 × 10 x 8 cm3 mass in the right kidney (Figure 2) consistent with RCC with a clot present in the IVC and extending into the thoracic IVC (2.5 cm below the right atrium (RA)) and the left renal vein.
Surgical approach entailed a full median sternotomy that was extended to a midline laparotomy. While the liver was being mobilized the patient was placed on CPB and allowed to reach deep hypothermia (16.5°). The liver was mobilized from its ligamentous attachments, leaving it connected only by the porta hepatis, the IVC, and the hepatic veins. An extended Cattell-Braasch and kocherization was performed to expose the retro- peritoneum and the intrahepatic IVC. At this stage, a strongly adhered IVC was apparent. It that the IVC. There was also significant lymphadenopathy around the renal hilum and underneath the IVC. The ureter and the gonadal veins were dissected. There were multiple parasitic vessels, which were clipped. The lower pole was then dissected, followed by the dissection of heavily adhered lymph nodes. Subsequently, the main renal vein and artery were identified and stapled. The adrenal gland was then dissected off the IVC, allowing for the removal of the kidney after releasing Gerota’s fascia.
At this stage the patient was placed on deep hypo- thermic circulatory arrest. A longitudinal 10 cm long incision was made in the IVC just below the liver in a juxtarenal location and cephalad to the IVC ligament behind the liver. The RA was also opened to aid in mobilizing the tumor thrombus superiorly. The ostium of the right renal vein was removed. There were several lumbar vessels and other branches that had tumor thrombus extending into them. These were completely declotted and then the orifices had to be oversewn from both inside and outside the IVC. Once all tumor thrombus was removed the IVC was re-anastomosed using a running 4-0 Prolene. After a circulatory arrest time of 26 min the patient was allowed to rewarm. As this occurred, more lymph nodes were resected from under the IVC. The RA was closed, patient was returned to normothermia, and weaned off CPB.
Pathology confirmed a diagnosis of pT3cN1 clear cell RCC with extensive rhabdoid and focal sarcomatoid differentiation, grade 4/4, tumor invasion into peri- nephric fat, renal sinus, and renal vein. Vascular re- section margin positive for malignancy. Thrombus of RCC in the IVC thrombus, and 1 of 7 lymph nodes was positive with extra-nodal extension. Given this
diagnosis, he was not eligible for conventional adjuvant therapy but was enrolled in the OZM-065 clinical trial and randomized to Arm A, consisting of pem- brolizumab and if progressive disease, pembrolizumab plus stereotactic body radiation therapy (SBRT). He initially had an excellent response to treatment, how- ever, developed immune-related colitis, and was re- moved from the trial. He received 8 cycles of treatment. On 4-years follow-up, the patient is symptom-free and living at home. He continues to be on surveillance for risk of RCC recurrence.
Patient 3: Adrenocortical carcinoma with IVC thrombus extending into the right atrium
A 62-year-old male who presented with 5-days history of dyspnea, diaphoresis, palpitations, presyncope, and epigastric pain. A CT scan (Figure 3) and MRI revealed a right adrenal mass measuring 5.4 x 4.9 × 4.2 cm3, a left renal mass measuring 5.5 x 4.5 x 3.6 cm3, and an IVC thrombus extending into the RA. His profile was also significant for autoimmune heparin-induced throm- bocytopenia (HIT), persistent thrombocytopenia of unknown etiology, and hypertension. Given the con- stellation of presenting symptoms and imaging findings, differential diagnosis included paraneoplastic syndrome and pheochromocytoma. Prior to surgery, the patient received 5 doses intravenous immune globulin (IVIG) and 4 doses of plasma exchange therapy (PLEX). Also, a negative HIT ELISA result was achieved before the surgery, circumventing the need to use argatroban or other heparin alternatives during CPB.
Surgical approach involved a full median sternotomy that was extended into a midline laparotomy. A Thompson-Farley retractor was placed to facilitate
exposure of the retroperitoneum, the right kidney, and the right adrenal gland. The liver was completely mo- bilized with control of the porta hepatis, infrahepatic IVC, and the suprahepatic IVC. Cattell-Braasch ma- neuver and kocherization of the duodenum were also performed to expose the kidney and allow for the ex- ploration of the IVC. Retroperitoneal lymph nodes in and around the IVC and the aorta were removed. With the bowels retracted, access to the left and right renal veins was achieved. Soft tissue dissection lateral to the gonadal vein facilitated the mobilization of the right kidney along the psoas fascia. The adrenal mass was intimately associated with the kidney. The superolateral and the superomedial aspects were then dissected. A few collateral vessels were present in this area that needed to be controlled. The adrenal mass and kidney, especially superomedially where the vessels entered, were chal- lenging to separate. To avoid getting into the adrenal mass for oncologic reasons, the upper pole of the kidney was skived. Unfortunately, there was some bleeding in this area, which was challenging to control. This was likely due to the high venous pressures related to caval obstruction. Multiple attempts were made to oversew the bleeding vessels, but to no avail. A clamp was also placed on the right renal artery, and although bleeding subsided, hemostasis was not achieved. Given the in- creasing operative time and the need to administer heparin prior to initiating CPB, ongoing blood loss would be highly likely. Therefore, a radical right ne- phrectomy was deemed to be safest option. The pos- sibility of auto-transplantation was considered. However, this was believed to be futile due to protracted ischemia time and insufficient renal artery, vein, and ureter.
The patient was cooled to deep hypothermia (17º) and CPB was instituted. The remainder of the adrenal
gland was mobilized around the hilum. Once circulatory arrest was initiated, a venotomy was made on the lateral aspect of the IVC around the insertion of the right adrenal vein ostium. The thrombus was carefully mo- bilized within the cava. The RA was opened to aid in thrombus mobilization superiorly. The IVC thrombus was removed in its entirety, and the caval wall was closed. After 20 min of circulatory arrest, the patient was rewarmed and weaned off CPB. There was slight bleeding at the level of the right renal vein and one of the short hepatic veins, both of which were oversewn with pledgeted sutures. FloSeal (Baxter, CA, USA), Surgicel (Adhezion Biomedical, PA, USA), Surgifoam (Ethicon, OH, USA), and Tisseel (Baxter, CA, USA) were put into the surgical bed to help control the medical bleeding. Upon removal of the bowel retractors, it was noted that the appendix appeared inflamed and injured. Therefore, it was removed along with the mesoappendix. Due to the complicated nature of the operation, the surgical team decided to postpone the management of the left renal mass to a later date pending the patient’s recovery. In total, the patient received 16 packs of red blood cells, 11 units of fresh frozen plasma, 3 units of platelets, and 3000 units of cryoprecipitate.
Biopsy of the left renal mass 10-weeks postoperatively confirmed a diagnosis of clear cell RCC. Repeat imaging at 7-months post-surgery revealed pulmonary nodules, lymphadenopathy in the right nephrectomy tumor bed, an enlarged lymph node medial to the IVC and superior to the nephrectomy bed, an enlarged lymph node posterior to the left renal vein, and a new enlarged lymph node in the surgical tumor bed on the right side. At this stage the patient received 10 rounds of palliative radiation therapy. 10 months after his surgery the pa- tient presented with 4-days history of progressive neurological loss affecting his legs. He was diagnosed to
have metastatic epidural soft tissue compression of the thoracic spinal cord at the T6 level. There was de- struction of the right T6 pedicle transverse process and lamina with extensive soft tissue extension. The patient underwent preoperative embolization of the right T6 and T7 radicular arteries. Subsequently, posterior T5-T7 decompression with partial vertebrectomy of T6 was performed along with pedicle screw instru- mentation T4-T8. He was then placed on palliative immunotherapy consisting of ipilimumab and nivolu- mab, which was complicated by pneumocystis jiroveci pneumonia. The patient passed away 15-months after his radical nephrectomy and IVC thrombectomy.
Patient 4: RCC with IVC thrombus extending into the right atrium
A 71-year-old male with a history of gastroesophageal reflux disease presented with 2-days of worsening post- prandial epigastric and right upper quadrant pain as- sociated with nausea, vomiting, and tachycardia. In- vestigations showed elevated liver enzymes and bilirubinemia. Abdominal imaging confirmed the presence of multiple gallstones in an otherwise normal- appearing gallbladder. There is no evidence of biliary dilatation, nor was there any pericholecystic edema or stranding to suggest the presence of acute inflammation. There was an incidental discovery of a right renal mass measuring 5.9 x 5.4 x 5.0 cm3, with thrombus present in the right renal vein and extending into the RA. He was diagnosed with choledocholithiasis and right RCC as- sociated with IVC thrombus.
Surgical approach involved an initial midline lapa- rotomy. A Thompson-Farley retraction system was used for optimal exposure. The liver was mobilized in its entirety requiring a small resection allowing it to be moved over to the midline. The hepato-caval ligament and right hepatic vein were isolated and divided. As this stage the abdominal IVC was exposed. An incision was made along the white line of Toldt and the posterior lower pole attachments of the kidney were dissected with the LigaSure. The duodenum was reflected me- dially along with the remaining small bowel. The main renal artery and vein were identified and divided. An accessory renal vein was identified below the main renal vein, which was also divided. The remaining attach- ments to the kidney were dissected while the adrenal gland was left in situ. Intraoperative transesophageal echocardiography confirmed the presence of tumor thrombus at the junction of the RA and the IVC.
A full median sternotomy was performed, and the patient was placed on CPB and allowed to cool to deep hypothermia (17º). Circulatory arrest was instituted and
the IVC was incised inferior to the RA and at the right renal vein ostium. The tumor thrombus was extracted en-bloc with the right kidney. The intrahepatic IVC was closed with a running 4-0 Prolene suture. After 9 min of circulatory arrest, circulation was reestablished, and as the patient was being rewarmed, a retroperitoneal lymph node dissection was performed with the nodal tissue posterior and lateral to the IVC. The operation was concluded with the repair of a hiatal hernia and a cholecystectomy. Pathology confirmed the diagnosis of clear cell RCC (pT3a pNX) and negative resection margins. Twenty-seven months post-surgery, the pa- tient continues to live independently and symptom-free at home.
Patient 5: RCC with thrombus extending into the intra-thoracic IVC and the gonadal vein
A 53-year-old male presented with 4-months history of worsening left flank pain. A CT scan revealed a large left renal mass measuring 18.8 × 10.3 × 9.0 cm3 associated with a tumor thrombus that extended into the renal vein, gonadal vein, and the IVC at the level superior to the hepatic vein. Four pulmonary nodules were also noted, 3 in the right lung (1 in each lobe) and 1 in the left lung. The patient was diagnosed to have metastatic malignant disease, with RCC as the most likely primary source.
Surgical approach involved a full median sternotomy that was extended to a midline laparotomy. A Thompson retraction system was used to optimize exposure. The right colon was mobilized inferiorly and a full kocherization was performed. The right liver was then mobilized to the midline. To access the IVC, due to severe inflammation surrounding the vein secondary to the thrombus, a partial hepatectomy was required. The IVC was entirely mobilized circumferentially superior to the insertion of the left renal vein. The right hepatic vein was encircled and controlled as well. The hepato-caval ligament was then divided. The left renal artery was identified, clipped, and ligated. Vesseloop was used to control and manipulate the IVC. Subsequently, the left kidney was then mobilized and excised in addition to the left renal vein. Tightening of the IVC vesseloop allowed for the excision of the affected portion of the IVC and the thrombus in one large cast. The open and thrombus- free IVC was flushed with heparinized saline. It was then reconstructed in the standard fashion using a combi- nation of Prolene sutures and graft as needed. Although preoperative planning included the potential need for CPB and deep hypothermic circulatory arrest, radical nephrectomy and complete IVC thrombectomy was achieved without them. Pathology confirmed the
diagnosis of clear cell RCC (pT3b pN0 pM1). Given the metastatic pulmonary nodules, immunotherapy was initiated 10-weeks post-surgery with ipilimumab and nivolumab. Patient was transitioned to maintenance therapy with nivolumab after 4-months. At 2-years follow-up, the patient remains symptom-free with no new metastases and stable pulmonary nodules.
Patient 6: Hepatocellular carcinoma (HCC) with thrombus extending into the IVC and the right atrium
A 75-year-old male presented to the emergency de- partment with acute onset right upper abdominal pain in the context of 5 kg unintentional weight loss over 1 month. His medical profile was otherwise significant for type 2 diabetes mellitus and rectal polyp carcinoma that was removed 7 years prior. An abdominal CT scan revealed a hypodense lesion in the left hepatic lobe with a suspected communication to a subcapsular collection in the anterior left hepatic lobe. There was also a filling defect in the left hepatic vein and the left portal vein. An abdominal MRI was performed, which showed a well- circumscribed lesion in the left hepatic lobe measuring 4.6 × 4.0 × 6.6 cm3 (Figure 4). A subcapsular collection, measuring 10 x 4 cm2, and suspicious for a hemorrhagic hepatic mass that had resulted from bleeding from the left hepatic artery and the left gastric artery was also noted. Further, the MRI demonstrated filling defect in the IVC and the RA, suggestive of a thrombus. An abdominal ultrasound study was subsequently per- formed, ruling out liver cirrhosis and portal hyperten- sion. Based on features on diagnostic imaging hepatocellular carcinoma (HCC) was the most likely diagnosis.
The patient underwent embolization of the left he- patic and gastric arteries to stabilize the hepatic he- matoma. Further work-up revealed coronary artery disease where the mid-left anterior descending (mLAD) artery had a 90% stenosis. The patient was scheduled to undergo left lateral sectionectomy, IVC thrombectomy, and coronary artery bypass graft surgery.
Surgical approach initially involved an upper midline incision. A Thompson-Farley retractor was placed to gain exposure. There was no evidence of liver or peri- toneal metastases. The adherent omentum and stomach were dissected off the left lobe of the liver as well as the anterior abdominal wall. The left lobe of the liver was completely mobilized by dissecting through the trian- gular ligaments to identify the underlying left hepatic vein and the IVC. Transection of the liver was per- formed by using the Aquamantys device (Medtronic, MN, USA) and electrocautery and scissors. The left
umbilical fissure was then encircled and the inflow to the 2 and 3 liver segments was then ligated using a TX 30 stapler (Ethicon, USA). Parenchymal transection was then commenced until the outflow of the origin of the hepatic veins was accessed. At this stage, a median full sternotomy was performed while the saphenous vein was harvested from the left leg. The IVC was completely exposed using the complete Cattell Braasch maneuver inferior to the renal vein. An umbilical tape was then placed around the inferior portion of the IVC distal to the infrarenal portion of IVC. The infrarenal IVC and the ascending aorta were then cannulated, and CPB was instituted. The patient was cooled to 16°. As the patient was being cooled to 16°, the rest of the liver parenchyma was transected. The left hepatic vein was completely isolated and opened. A tumor thrombus was noted. The mobilized segments of the left liver were resected, leaving the left hepatic vein stump and the thrombus in situ. With complete circulatory arrest, the RA was opened, and the tumor thrombus was visualized from within the RA into the IVC, which was then pushed down. With gentle maneuvering, the tumor thrombus was resected completely and intact. No residual thrombus was noted in the left hepatic vein or in the IVC. The left hepatic vein and the RA were closed with 5-0 Prolene. As the patient was being rewarmed, the harvested saphenous vein was used to bypass the mLAD artery. Heart function was normal, so patient was weaned from CPB, and the sternum was closed in standard fashion. However, the patient was coagulo- pathic, so the abdomen was packed but left open, and the patient was taken to the intensive care unit for continued physiological support. Having stabilized overnight, the patient was returned to the operating
room the next day where his abdomen was closed. Post- operatively, the patient suffered a cerebrovascular event resulting in left hand weakness and dysphagia. However, he had no residual neurological deficits upon discharge. He was discharged to home on post-operative day 17.
Discussion
Tumors involving the IVC usually arise from organs that have direct venous drainage into the IVC, such as the liver and the kidneys. The presence and extent of an IVC thrombus vary based on the location of the primary source and timing of finding. Management of the pri- mary tumor and IVC tumor thrombus may include radiation therapy, immunotherapy, surgery, or combi- nation therapy.15-21 Although major strides have been made in the non-operative approaches to these malig- nancies, surgical excision is usually indicated to facilitate improved outcomes. In the present study we have re- ported the outcomes of surgical IVC thrombectomy for a series of 6 patients. Three patients had clear cell RCC, while 1 had adrenocortical carcinoma with IVC thrombus extending into the right atrium, 1 had a retroperitoneal leiomyosarcoma, and 1 had HCC. Surgical IVC thrombectomy was successful for all 6 patients. However, the patient with the adrenocortical carcinoma experienced a complicated post-operative course that was exacerbated by aggressive metastatic disease.
Complimenting the current literature, our center’s experience with surgical IVC thrombectomy adds further insight into the post-surgical outcomes for these patients. Haddad et al reported the long-term surgical outcomes of patients with RCC in whom IVC thrombus was present.22 This multicenter study, which included 166 patients and the median follow-up was 27.8 months, found that contemporary surgical management achieved almost 50% 5-years survival in RCC patients with IVC thrombus but without distant metastases.22 Factors that were as- sociated with increased mortality included nodal metastases and advanced tumor grade. In another single-center study of 15 patients with RCC and IVC tumor thrombus involvement, who underwent radical nephrectomy and IVC thrombectomy, revealed a 1- year survival rate of 93%.23 Tsuji et al. also reported the long-term outcomes of 33 patients who had RCC with IVC tumor extension.24 This single-center study found that the overall 1-, 5-, and 10-years survival rates were 70%, 44%, and 26.4%. Importantly, the authors also showed that 1- and 5-years survival rates were 81.3% and 52.9% for Stage III and 50% and 31.2% for Stage IV IVC tumors. Indeed, a statistically
significant correlation was noted between surgical staging and survival rates. With respect to HCC and IVC tumor thrombus, 1- and 3-years survival rates have ranged from 29.2%-80% and 15.4%-33.1%, re- spectively, for patients who underwent surgical thrombectomy.25 It is believed that outcomes for patients with HCC will further improve with the emergence of immunotherapy-based strategies. Transcatheter arterial chemoembolization (TACE) is an important option that is indicated for non-surgical patients and palliative cases.2 25
Patients presenting with tumors or thrombi in the IVC are usually complex. These patients should be managed by a multidisciplinary team consisting of cardiovascular surgeons, hepatobiliary surgeons, urol- ogists, medical oncologists, and radiation oncologists. A personalized treatment plan must be devised so that neoadjuvant and adjuvant therapeutics are tailored for each patient. Preoperative planning should also be comprehensive where multimodality imaging should be used to accurately characterize the tumor and extent of IVC involvement. Finally, given the often challenging and multifaceted nature of these cases, operative strategy should be carefully conceived. Our study shows that favorable surgical outcomes can be achieved for those with tumors and thrombi affecting the IVC. A limitation of this manuscript is the small sample size. Since the same group of surgeons performed the operations, it is difficult to determine the learning curve that is required to ensure optimal surgical outcomes for this patient population.
Conclusion
Tumors affecting the IVC can originate from the IVC or from surrounding organs, such as the kidneys and the liver. In some cases, tumor thrombus involving the IVC can extend into the right atrium. Although adjunct therapies, including radiation therapy and chemother- apy, will continue to have a role in the management of patients presenting with IVC tumor thrombi, surgical resection is usually indicated. Depending on extent and level of IVC involvement, cardiopulmonary bypass and deep hypothermic circulatory arrest may be needed. Our case series suggests that a multidisciplinary approach to these tumors can facilitate excellent clinical outcomes. Further larger studies are required to establish the long- term outcomes of surgical IVC thrombectomy.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical approval
This study was approved by the Institutional Ethics Research Board.
ORCID iD
Ali Fatehi Hassanabad ® https://orcid.org/0000-0003-0650- 0260
Supplemental Material
Supplemental material for this article is available online.
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