Original communications
Adrenocortical carcinoma extending into the inferior vena cava: Presentation of a 15-patient series and review of the literature
Laurent Chiche, MD,a Bertrand Dousset, MD,b Edouard Kieffer, MD,a and Yves Chapuis, MD,b Paris, France
Background. Involvement of the inferior vena cava (IVC) is a controversial risk factor for surgical treatment of adrenocortical carcinoma (ACC). This study aims to assess the outcome of an aggressive surgical policy for ACC extending into the IVC and discuss treatment strategies based on a review of the literature.
Methods. Over a 25-year period, 15 patients were treated for ACC extending into the IVC. The upper limit of the extension was the infrahepatic IVC in 2 patients, retrohepatic IVC in 6, and suprahepatic IVC in 7, including 4 with extension into the right atrium. Seven patients presented with concurrent metastases. The operative technique was thrombectomy (n = 13), partial resection with direct closure (n = 1), and total resection with replacement of the IVC (n = 1). Venous control was achieved by caval clamping alone (n = 4), hepatic vascular exclusion (n = 5), and the use of normothermic cardiopulmonary bypass or hypothermic circulatory arrest (n = 6).
Results. Two patients died postoperatively. Ten patients died of metastatic complications at 4 to 31 months. Median survival time was 8 months. Three patients were still alive after 24, 25, and 45 months of follow-up, one of whom was reoperated at 17 months for a local recurrence. No evidence of recurrent intravenous involvement was found during follow-up in any patient in whom complete resection was achieved.
Conclusions. Our findings suggest that surgical treatment can be effective for management of ACC with extension into the IVC. Long-term prognosis is poor owing to delay in diagnosis, frequent associated metastatic disease and lack of effective adjuvant treatment. (Surgery 2006;139:15-27.)
From the Department of Vascular Surgery,” Pitié-Salpêtrière University Hospital and the Department of Visceral Surgery, Cochin University Hospital, Assistance Publique-Hôpitaux de Paris
ADRENOCORTICAL CARCINOMA (ACC) is a rare malig- nancy. Poor prognosis is related to delay in diag- nosis and to the lack of effective adjuvant treatment.2-5 Although prognostic factors are un- clear, several studies6-9 indicate that curative surgi- cal resection can improve survival rate. No study has conclusively found that intravenous extension
Accepted for publication May 20, 2005.
Reprint requests: Laurent Chiche, MD, Department of Vascular Surgery, Pitié-Salpêtrière University Hospital, 47-83 Bd. de l’Hô- pital, 75013 Paris, France. E-mail: laurent.chiche@psl.aphp.fr.
0039-6060/$ - see front matter
doi:10.1016/j.surg.2005.05.014
is a poor prognostic feature. Involvement of the in- ferior vena cava (IVC) was first reported in 1972.10 Since then, only single case reports and small se- ries have been published. We describe our experi- ence in a series of 15 patients and review the literature to determine the feasibility and efficacy of complete surgical resection for ACC extending into the IVC.
METHODS
From August 1977 to October 2002, 105 pa- tients underwent surgical treatment for ACC at our institutions. Twenty-six (24.8%) presented with extension into the adrenal vein, renal vein, or IVC. This retrospective study describes the surgical management of all 15 patients (14.3%) with major
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IVC extensions. Some of them already have been included without description in a previous re- port.11 There were 10 women and 5 men, with a mean age of 45.9 ± 19.3 years (range, 15 to 80 years). The clinical symptoms of excess steroid pro- duction (Cushing’s syndrome) were isolated in 7 patients and associated with less specific manifesta- tions in 8 (abdominal mass or pain, fever, weight loss, and fatigue). Five patients presented with bi- lateral edema of the lower extremities including one with bilateral phlebitis. Bilateral pulmonary embolism was the presenting disorder in one pa- tient (Fig 1). The mean delay between onset of symptoms and diagnosis was 11.3 months (range, 0 to 48 months). The delay in diagnosis was less than 3 months in 8 patients. Two patients were considered high-risk cases for surgery including one with chronic cardiac failure and one with por- tal hypertension owing to cirrhosis with portal vein thrombosis and hypersplenism.
The primary ACC was located on the right side in 12 patients and left in 3 (Table I). In our overall series of 105 patients, these patients accounted for 21% (12/56) with right-sided tumors and 6% (3/ 49) with left-sided tumors. Based on data available for all but 2 patients, mean tumor weight was 1,154 g (range, 190 to 3100 g). Maximum tumor diame- ter ranged from 8 to 22 cm. Nine tumors were greater than 15 cm in diameter. Hormone assays showed 9 functioning and 6 nonfunctioning ACC.
Depending on the date of treatment, assess- ment of the primary tumor and its local or meta- static extensions was carried out by abdominal Doppler ultrasound, transesophageal echocardiog- raphy, cavography, computed tomography (CT) scan (Fig 2), or magnetic resonance imaging (MRI; Fig 3). Right ACC appeared generally as a hetero- geneous necrotic soft tissue mass extending be- hind the liver toward the diaphragm and IVC and pushing the kidney downward. Left ACC usu- ally was associated with anterior displacement of the pancreas and spleen and posterior displace- ment of the kidney. Accurate assessment of the dis- tal limit of caval involvement was best achieved by the combination of Doppler ultrasound, transeso- phageal echocardiography, and MRI in recent cases, whereas cavography was used in earlier cases.
We classified patients into 3 groups using crite- ria similar to those proposed for caval involvement associated with renal carcinoma.12 The upper limit
Fig 1. A, Cavography shows tumor thrombus extending to the cavoatrial junction. B, Angiography in the same patient shows major obstruction of the right pulmonary artery after migration of tumor thrombus.
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120 KV 140 MA LRG SFOV 5 0 MM
| No. | Age/sex | Side | Caval extension | Stage | Surgical approach | Method of treatment | Venous control | Follow-up |
|---|---|---|---|---|---|---|---|---|
| 1 | 44/M | Right | A | IV | Subcostal + ME | Thrombectomy | Cross-clamping | Died, 17 mo |
| 2 | 33/F | Left | A | IV | Subcostal | Thrombectomy | Cross-clamping | Died, 7 mo |
| 3 | 80/F | Right | B | IV | Subcostal + ME | Thrombectomy | Cross-clamping | Died, 6 mo |
| 4 | 46/F | Right | B | III | Thoracoabdominal | Thrombectomy | HVE | Died, 4 mo |
| 5 | 34/F | Right | B | III | Subcostal + TP | Thrombectomy | HVE | Died, 11 mo |
| 6 | 26/F | Right | B | IV | Subcostal + ME | Resection-graft* | HVE | Died, 31 mo |
| 7 | 72/M | Left | B | III | Sternolaparotomy | Thrombectomy | HCA | Died, 1 d |
| 8 | 45/M | Left | B | III | Subcostal + ME | Thrombectomy | HVE | Alive, 24 mo |
| 9 | 73/M | Right | C | IV | Subcostal | Thrombectomyt | Cross-clamping | Died, 6 mo |
| 10 | 23/F | Right | C | IV | Subcostal + TP | Resection | HVE | Died, 6 mo |
| 11 | 44/F | Right | C | IV | Subcostal + MS | Thrombectomy | Normothermic CPB + HVE | Died, 8 mo |
| 12 | 15/F | Right | C (RA) | III | Sternolaparotomy | Thrombectomy | HCA | Died, 8 mo |
| 13 | 53/F | Right | C (RA) | III | Subcostal + MS | Thrombectomy | Normothermic CPB + HVE | Alive, 45 mo |
| 14 | 65/M | Right | C (RA) | III | Subcostal + MS | Thrombectomy | HCA | Died, 30 d |
| 15 | 36/F | Right | C (RA) | III | Sternolaparotomy | Thrombectomy | HCA | Alive, 25 mo |
Caval extension [Kearney et al12]: A, infrahepatic vena cava; B, retrohepatic vena cava; C, suprahepatic vena cava; RA, right atrium; TP, thoracophrenotomy; ME, median extension, MS, median sternotomy; HVE, hepatic vascular exclusion; CPB, cardiopulmonary bypass; HCA, hypothermic circulatory arrest.
*Polytetrafluoroethylene.
+Partial thrombectomy.
of caval extension was located below the liver (ex- tent A) in 2 patients, behind the liver (extent B) in 6, and above the liver (extent C) in 7 including 4 with extension into the right atrium. Extension consisted of endoluminal tumor thrombus in 14 patients (including 3 with associated parietal in- volvement) and invasion of the venous wall without
thrombus in one. In the overall series of 105 pa- tients, invasion of the IVC was observed in 14.3% (15 of 105) and involvement of the right atrium in 3.8% (4 of 105). Thrombosis of the infrarenal IVC was seen in 2 patients.
Seven patients presented with lung (n = 3) or liver (n = 4) metastases. According to the system
proposed by MacFarlane13 and modified by Sulli- van et al,14 8 patients with associated local or lymph node involvement without metastasis were classified as stage III. Seven patients with concur- rent metastases were classified as stage IV.
Surgical treatment was undertaken not only if total resection was deemed feasible but also to prevent the risk of pulmonary embolism, reduce the clinical effects of hormonal hypersecretion, and relieve symptomatic compression of surround- ing organs by large tumors. Right ACC was ex- posed by the bilateral subcostal approach in 9 patients in association with a vertical midline abdominal incision in 3 cases, sternotomy in 3 cases, and thoracotomy in 2 cases. In the remain- ing 3 patients with right ACC, exposure was achieved by thoracoabdominal incision. Left ACC was exposed by the bilateral subcostal route in 2 patients and by midline sternolaparotomy in 1.
Total resection of the primary tumor and ex- tension was achieved in a curative intent in 12 patients. Surgery was indicated in a palliative intent, and resection was incomplete in 3 patients
with pulmonary metastasis. In one of them, gen- eral status was so poor that complete excision of a huge tumor was unfeasible, and the kidney showing macroscopic involvement had to be left in place. Adrenalectomy was associated with ipsi- lateral nephrectomy in 11 patients and indicated for macroscopic tumoral involvement in 10 and ischemia after tumor resection in 1. Lymphade- nectomy was performed in all patients. In 4 patients, partial hepatectomy was performed to remove metastases or local spreading. Hepatec- tomy included segment V in 1 patient, segments II and III in 1 patient, segments V, VI, VII, and VIII in 1 patient, and segments V, VI, VII, VIII and the caudate lobe in 1 patient.
Surgical technique varied depending on type and location of tumor involvement. Thrombec- tomy was performed in 13 patients. The upper limit of the extension into the IVC was located below the suprahepatic veins in 7 patients and above in 6. In the first group, venous control was achieved by cross clamping of the IVC in 3 patients, by hepatic vascular exclusion (HVE) including
cross clamping of the IVC above and below the liver and clamping of the portal triad in 3 patients, and by cardiopulmonary bypass (CPB) with hypother- mic circulatory arrest (HCA) in 1 patient present- ing thrombosis of the portal vein. In the second group, CPB was used in 5 of 6 cases. In 2 patients, the procedure performed under normothermic conditions consisted of total thrombectomy of the retrohepatic IVC by right atriotomy and suprarenal cavotomy under HVE followed by resection of the primary tumor. One of them also had bilateral pulmonary embolectomy. In the 3 remaining cases involving CPB, total thrombectomy of the retro- hepatic and suprahepatic IVC was achieved under HCA by anterior suprarenal cavotomy followed by vertical atriotomy to allow the intra-atrial portion of thrombus to be pushed down to the cavotomy. Dissection and removal of the primary tumor were performed during rewarming, after heparin rever- sion and discontinuation of CPB. In the remaining patient presenting with suprahepatic caval throm- bosis, venous control was achieved by cross clamp- ing of the intrapericardial IVC. The procedure consisted of incomplete thrombectomy and partial adrenalectomy after cross clamping. In 2 of the 4 patients operated on under HCA, ligation of the infrarenal IVC occluded by cruoric thrombus was performed without reconstruction. In 11 of the 13 thrombectomies, the cavotomy was closed by direct suture. In the 2 remaining cases, a polytetrafluoro- ethylene (PTFE) patch was used to enlarge the interrenal IVC or the junction between the IVC and suprahepatic veins.
Thrombectomy was not performed in 2 pa- tients. One woman presenting with involvement of the retro and suprahepatic wall of the IVC with no tumoral thrombus was treated by partial resection of the IVC followed by direct closure. Venous control was achieved by HVE. The other patient who did not undergo thrombectomy presented with suprarenal, retrohepatic involvement of the IVC that was treated by segmental resection of the IVC under HVE with intrapericardial clamping of the IVC. Vascular continuity was re-established with a 20-mm-diameter PTFE graft.
RESULTS
Two patients presenting with stage III ACC, including 1 with cirrhosis and portal thrombosis, died of multiple organ failure after caval throm- bectomy performed under HCA. Renal infarction developed in another patient who presented with hemorrhage 2 days after the procedure, which required nephrectomy. The most likely cause was complete thrombosis of the prosthetic graft used
to replace the IVC. No attempt was made to thrombectomize. Postoperative recovery was un- eventful. No embolic or major complications were observed in any of the other 12 patients. Minor complications occurred in 6 patients (parietal hematoma or infection in 3 cases, pleural or pericardial effusion in 2 cases, intestinal occlusion requiring reintervention for adhesiolysis in 1 case).
Histologic diagnosis was performed based on widely accepted criteria4 including tumor size greater than 5 cm, tumor weight greater than 150 g, structural abnormalities, tumor cell necro- sis, calcification, mitotic activity, nuclear polymor- phism, adenopathy, and vascular involvement. Findings were always compatible with ACC. In 8 of 11 patients who underwent en bloc resection of the adrenal gland and kidney, histologic find- ings showed no evidence of tumoral invasion of the kidney. Involvement of the liver was confirmed in the 4 patients in whom hepatectomy was com- bined with adrenalectomy. Macroscopically, the thrombus removed from the IVC was soft, friable, laced with necrotic cells, and sometimes encapsu- lated in thin cream-colored conjunctive tissue. His- tologic analysis of thrombus from the IVC and pulmonary arteries was always consistent with intra- venous extension of ACC.
After surgical resection, all surviving patients underwent adjuvant chemotherapy with mitotane (3 to 12 g/d).5 The combination of surgery and mitotane therapy was effective in reducing hor- mone levels postoperatively in all patients with functioning tumors. No patients received radiation therapy.
Mean follow-up of the 13 operative survivors was 15.3 ± 12.5 months (range, 4 to 45 months). Ten patients died of tumor-related complications. Me- dian survival time was 8 months. The 3 patients in whom surgical treatment was considered to be incomplete died at 6, and 8 months of complica- tions related to progression of residual tumor. Seven of the 10 patients in whom surgical resection was considered as curative died within 4 to 31 months of metastatic progression appearing be- tween 3 and 9 months postoperatively. Two pa- tients were still alive with no sign of local recurrence or metastasis at 24 and 45 months. Local recurrence was observed in 1 patient at 15 months. Reintervention was performed at 17 months, and the patient was still alive with no sign of local recurrence or metastasis at 25 months. No clinical or radiologic evidence of recurrent intravenous involvement was found during follow- up in any patient in whom complete resection was achieved.
| No. | Study | Year | Age/ sex | Side | Caval extension | Surgical approach | Method of treatment | HVE/ CPB | Follow-up |
|---|---|---|---|---|---|---|---|---|---|
| 1 | Castleman et al10 | 1972 | 7/M | Right | B | NM | Thrombectomy | HVE | Died peroperatively |
| 2 | Proye et al17 | 1973 | NM/F | Left | A | Thoracoabdominal | Thrombectomy | NM | Alive, 5 mo |
| 3 | Shons and | 1974 | 77/F | Right | C (RA) | None | Died before | ||
| Gamble18 | surgery | ||||||||
| 4 | Scully et al15 | 1976 | 37/M | Right | C (RA) | Sternolaparotomy | Resection | CPB | Died |
| peroperatively | |||||||||
| 5 | Cahill and Sukov1 | 1977 | 67/F | Right | A | NM | Thrombectomy | NM | Alive, 5 mo |
| 6 | Cahill and Sukov19 | 1977 | 25/F | Left | NM | NM | NM | NM | Died, 13 mo |
| 7 | Cahill and Sukov19 | 1977 | 65/F | Left | NM | NM | NM | NM | Died, 2 mo |
| 8 | Cahill and Sukov | 1977 | 27/F | Right | NM | NM | NM | NM | Alive, 6 mo |
| 9 | Cahill and Sukov19 | 1977 | 43/F | Right | NM | NM | NM | NM | Died, 26 mo |
| 10 | Cahill and Sukov19 | 1977 | 51/F | Right | NM | NM | NM | NM | Alive, 48 mo |
| 11 | Cahill and Sukov19 | 1977 | 33/M | Right | NM | NM | NM | NM | Alive, 21 mo |
| 12 | Javadpour et al20 | 1978 | 22/F | Right | B | Thoracoabdominal | Thrombectomy | HCA | Alive, 12 mo |
| 13 | Dunnick21- Geelhoed22 | 1980 | 22/F | Right | C | Sternolaparotomy | Thrombectomy | CPB | Alive, 36 mo |
| 14 | Dunnick21- Geelhoed22 | 1980 | 23/F | Left | A | NM | Thrombectomy | No | Alive, 22 mo |
| 15 | Dunnick21- Geelhoed22 | 1980 | 27/M | Left | B | Sternolaparotomy | Thrombectomy | No | Alive, 24 mo |
| 16 | Martorana et al23 | 1981 | 45/F | Left | A | Subcostal | Resection | NM | Alive, 5 mo |
| 17 | Henley et al24 | 1983 | NM/ NM | NM | NM | NM | Thrombectomy | NM | NM |
| 18 | Smith et al25 | 1984 | 38/F | Right | B | Subcostal + MS | Resection | HVE | Alive, 9 mo |
| 19 | Schramek et al26 | 1985 | 52/F | Right | C (RA) | NM | Thrombectomy* | NM | Died, 5 mo |
| 20 | Hugh et al27 | 1986 | 18/F | Right | C (RA) | Sternolaparotomy | Thrombectomy | No | Died, 14 mo |
| 21 | Hugh et al27 | 1986 | 43/F | Right | C (RA) | Sternolaparotomy | Thrombectomy | CPB | Alive, 15 mo |
| 22 | Ritchey et al28 | 1987 | 44/M | Right | A | Median laparotomy | Biopsy | Died, 10 mo | |
| 23 | Ritchey et al28 | 1987 | 57/F | Right | A | NM | Thrombectomy | NM | Alive, 6 mo |
| 24 | Ritchey et al28 | 1987 | 60/F | Right | B | NM | Thrombectomy | NM | Alive, 12 mo |
| 25 | Braband and | 1987 | 72/F | Right | B | Thoracoabdominal | Thrombectomy | NM | Died, 3 mo |
| Soreide29 | |||||||||
| 26 | Pritchett et al30 | 1987 | 72/F | Right | C (RA) | Thoracoabdominal | Thrombectomy | NM | NM |
| 27 | Falke et al31 | 1988 | 56/F | Left | C (RA) | Thoracoabdominal | Thrombectomy* | NM | NM |
| 28 | Carbonnel et al32 | 1988 | 28/F | Right | C | NM | Thrombectomy | CPB | Died, 2 d |
| 29 | Bodie et al33 | 1989 | NM/ | NM | NM | NM | NM | NM | NM |
| to | NM | ||||||||
| 33 |
| No. | Study | Year | Age/ sex | Side | Caval extension | Surgical approach | Method of treatment | HVE/ CPB | Follow-up |
|---|---|---|---|---|---|---|---|---|---|
| 34 | Shahian et al16 | 1989 | 51/F | Right | C (RA) | Subcostal + MS | Thrombectomy | HCA | Alive, 10 mo |
| 35 | Cheung et al34 | 1989 | 22/F | Right | C (RA) | Subcostal + MS | Thrombectomy | HCA | Died, 12 mo |
| 36 | Godine et al35 | 1990 | 13/F | Right | C (RA) | Thoracoabdominal | Thrombectomy | CPB | NM |
| 37 | Godine et al35 | 1990 | 2/F | Left | C (RA) | Subcostal | Thrombectomy | NM | Died, |
| peroperatively | |||||||||
| 38 | Godine et al35 | 1990 | 17/F | Right | C (RA) | None | Died, 9 mo | ||
| 39 | Prando et al36 | 1990 | NM/ | NM | NM | NM | NM | NM | NM |
| to | NM | ||||||||
| 40 | |||||||||
| 41 | Moul et al37 | 1991 | 33/M | Left | C | Subcostal + MS | Thrombectomy | CPB | Alive, 36 mo |
| 42 | Schwartz® 38 | 1991 | 34/F | Right | B | NM | Resection-Graftț | HVE | Alive, 12 mo |
| Miller39 | |||||||||
| 43 | Concepcion et al40 | 1991 | 38/F | Right | C (RA) | Subcostal + MS | Thrombectomy | NM | Died, 18 mo |
| 44 | Concepcion et al40 | 1991 | 27/F | Right | C (RA) | Sternolaparotomy | Thrombectomy | CPB | Alive, 17 mo |
| 45 | Concepcion et al40 | 1991 | 55/F | Right | C (RA) | Sternolaparotomy | Thrombectomy | CPB | Alive, 12 mo |
| 46 | Decker and Kuehner | 1991 | 41/F | Right | C (RA) | NM | NM | NM | Died, 21 mo |
| 47 | Decker and | 1991 | 48/F | Right | B | NM | NM | NM | Died, 2 mo |
| Kuehner41 | |||||||||
| 48 | Stewart et al42 | 1991 | 26/F | Right | C | Sternolaparotomy | Thrombectomy | CPB | Alive, 17 mo |
| 49 | Stewart et al42 | 1991 | 55/F | Right | C | Sternolaparotomy | Thrombectomy | CPB | Alive, 29 mo |
| 50 | Stewart et al42 | 1991 | 38/F | Right | C | Sternolaparotomy | Thrombectomy | CPB | Died, 15 mo |
| 51 | Icard et al4§ | 1992 | NM/ | NM | NM | NM | 5 | NM | NM |
| to | NM | Thrombectomies | |||||||
| 62 | |||||||||
| 7 lat. wall | |||||||||
| resections | |||||||||
| 63 | Spay43 | 1993 | 58/F | Right | A | Median laparotomy | Resection | NM | Died, 8 mo |
| 64 | Galli et al44 | 1994 | NM/ | Right | C | Sternolaparotomy | Thrombectomy | HCA | NM |
| NM | |||||||||
| 65 | Siegelbaum et al45 | 1994 | 23/F | Right | B | Thoracoabdominal | Resection | No | Alive, 60 mo |
| 66 | Siegelbaum | 1994 | 72/F | Left | B | Subcostal + MS | Thrombectomy | CPB | Died, |
| et al45 | peroperatively | ||||||||
| 67 | Huguet46_ Huguet47 | 1994 | 21/M | Right | C (RA) | Thoracoabdominal | Resection | HVE | Died, 4 mo |
| 68 | Friedrich et al48 | 1994 | 47/F | Right | C (RA + RV) | NM | Resection-Graftt | HCA | Alive, 36 mo |
| 69 | Virseda | 1994 | 50/F | Left | A | Median laparotomy | Thrombectomy | No | Alive, 36 mo |
| Rodriguez et al49 | |||||||||
| 70 | Wei et al50 | 1995 | 53/F | Left | A | Sternolaparotomy | Thrombectomy | CPB | Alive, 2 mo |
| 71 | Lee et al6 | 1995 | NM/ | NM | NM | NM | NM | NM | NM |
| to | NM | ||||||||
| 74 | |||||||||
| 75 | Huguet et al47 | 1995 | 56/M | Right | B | NM | Resection-Graftt | HVE | Died, 5 d |
| 76 | Baumgartner et al51 | 1996 | 43/M | Right | A | Thoracoabdominal | Thrombectomy | VVB | NM |
| 77 | Mingoli et al52 | 1996 | 28/F | Left | A | Subcostal | Thrombectomy | No | Died, 7 mo |
| 78 | Figueroa et al' | 1997 | 54/F | Right | C (RA) | Thoracoabdominal | Thrombectomy | NM | Alive, 12 mo |
| No. | Study | Year | Age/ sex | Side | Caval extension | Surgical approach | Method of treatment | HVE/ CPB | Follow-up |
|---|---|---|---|---|---|---|---|---|---|
| 79 | Figueroa et al53 | 1997 | 35/M | Right | B | Thoracoabdominal | Thrombectomy | NM | Alive, 60 mo |
| 80 | Figueroa et al53 | 1997 | 14/F | Right | B | Thoracoabdominal | Thrombectomy | NM | Alive, 72 mo |
| 81 | Figueroa et al53 | 1997 | 41/F | Right | C (RA) | Thoracoabdominal | Thrombectomy | NM | Died, 60 mo |
| 82 | Figueroa et al53 | 1997 | 57/M | Right | B | Thoracoabdominal | Thrombectomy | NM | Died, 8 mo |
| 83 | Yamana et al54 | 1997 | 38/M | Left | C (RA) | NM | Thrombectomy | CPB | NM |
| 84 | Hedican and Marshall55 | 1997 | 51/M | Right | B | Thoracoabdominal | Thrombectomy | HCA | Alive, 80 mo |
| 85 | Hedican and Marshall55 | 1997 | 29/F | Right | C (RA) | Thoracoabdominal | Thrombectomy | HCA | Died, 8 mo |
| 86 | Hedican and Marshall55 | 1997 | 52/F | Right | A | Thoracoabdominal | Thrombectomy | No | Died, 8 mo |
| 87 | Lee et al56 | 1998 | 26/F | Left | C (RA) | NM | Thrombectomy | CPB | Alive, 21 d |
| 88 | Boneschi et al57 | 1998 | 50/M | Left | C (RA) | Median laparotomy | Biopsy | NM | Died, 2 mo |
| 89 | Peix et al58 | 1998 | 58/F | Left | B | NM | Thrombectomy | NM | NM |
| 90 | Peix et al58 | 1998 | 23/F | Right | B | NM | Resection | NM | Died, 40 mo |
| 91 | Peix et al58 | 1998 | 39/M | Right | C (RA) | NM | Thrombectomy | CPB | Alive, 31 mo |
| 92 | Peix et al58 | 1998 | 50/M | Right | B | NM | Resection | NM | Alive, NM |
| 93 | Peix et al58 | 1998 | 63/F | Right | A | NM | Thrombectomy | NM | NM |
| 94 | Tritos et al59 | 2000 | NM | NM | NM | NM | NM | NM | NM |
| to | |||||||||
| 99 | |||||||||
| 100 | Ribeiro et al60 | 2000 | NM | Right | A | NM | NM | NM | NM |
| 101 | Salinas Sanchez et al61 | 2000 | 36/F | Right | C (RA) | Sternolaparotomy | Thrombectomy | CPB | Alive, 13 mo |
| 102 | Langer et al62 | 2000 | NM | NM | NM | NM | NM | NM | NM |
| to | |||||||||
| 103# | |||||||||
| 104 | Chesson and Theodorescu | 2002 | 59/F | Left | C (RA) | NM | Thrombectomy | HCA | NM |
| 105 | Radecka et al64 | 2003 | 60/M | Left | C, RA | NM | Thrombectomy | HCA | NM |
| 106 | Ortiz Gorraiz et al65 | 2003 | 52/M | Left | A | Subcostal ME | Thrombectomy | No | Died, 2 mo |
NM, Not mentioned; Caval extension [Kearney et al12]: A, infrahepatic vena cava; B, retrohepatic vena cava; C, suprahepatic vena cava; RA, right atrium; RV, right ventricle; TP, thoracophrenotomy; ME, median extension, MS, median sternotomy; HVE, hepatic vascular exclusion; CPB, cardiopulmonary bypass; HCA, hypothermic circulatory arrest; VVB, venovenous bypass.
*Partial thrombectomy.
+Polytetrafluoroethylene.
¿Superficial femoral vein.
§This multicentric study may have included some of the same cases as other reports17,43,58 and the present series.
“In this series, follow-up was not specifically described: died, 2 patients (13 and 40 mo), alive (9, 13, and 31 mo).
These 2 patients had tumoral caval thrombus as local recurrences 5 and 10 months after initial surgery.
DISCUSSION
The diagnostic and therapeutic pitfalls specific to ACC extending into the IVC were described as early as 1972.1º Use of CPB techniques to facilitate tumor resection in patients with caval involvement was reported 4 years later.13 In 1989, Shahian
et al16 reported the first procedure using CPB with HCA.
Based on extensive perusal of the litera- ture, 4,6,10,15-65 we compiled 106 sufficiently de- tailed cases involving patients presenting ACC with IVC extension. Including our patients, this
brings the number of cases suitable for analysis to 121. Because some cases have not been reported or specifically described in large series, the inci- dence of ACC with IVC involvement may be underestimated.
Table II presents the features and outcomes of the 106 patients described in the literature. The side of the lesion was the right in 54 cases, left in 20, and not mentioned in 32. The upper limit of involvement was the infrahepatic IVC in 15 cases, retrohepatic IVC in 18, suprahepatic IVC in 35 (in- cluding 27 cases of right atrial involvement and 1 of right ventricular involvement), and not men- tioned in 38. The therapeutic option consisted of surgical resection in 76 patients, surgical biopsy without resection in 2, and not mentioned in 28. The surgical approach was specified in 44 cases. Unilateral or bilateral subcostal laparotomy was used in 10 cases (isolated in 4 and in association with median sternotomy in 6), median laparotomy in 4, and median sternolaparotomy in 13. In the remaining 17 cases, the approach was described as “thoracoabdominal.” The treatment of intrave- nous involvement in the 76 surgical patients was thrombectomy in 56 cases, lateral or total parietal resection of the IVC without reconstruction in 15, resection of the IVC with graft replacement in 3, and biopsy without resection owing to inoper- ability in 2. A venous control technique other than cross clamping was described in 32 patients includ- ing HVE in 5 cases, venovenous bypass in 1 case and CPB in 26 cases including 6 under HCA. Out- come was described in 65 patients. Seven patients died before or during the postoperative period. Twenty-four patients died during follow-up after a mean survival time of 13.2 ± 13.6 months (range, 2 to 60 months) and a median survival time of 9 months. Ten of these patients (43%) survived at least 12 months. Thirty-four patients were alive with metastasis or no evidence of recurrence after a mean follow-up of 23.1 ± 20.4 months (range, 1 to 80 months). Twelve of these patients (35%) survived at least 24 months.
Massive involvement of the IVC is generally considered a limiting factor for resection of retro- peritoneal tumors.66,67 Because of the poor prog- nosis of these tumors and technical difficulties related to venous control and vascular reconstruc- tion, radical surgical resection is controversial. As we noted, ACC invaded adjacent and retroperito- neal organs in about 25% of cases. ACC can affect the IVC by either compression or direct invasion or by intraluminal extension in the form of thrombus (usually without attachment to the venous wall).68 The length of the left renal vein probably explains
why IVC extension is more commonly observed with right-sided ACC. Tumor thrombus can subse- quently cross the cavoatrial junction and progress into the right atrium.68 Extension to the tricuspid valvular plan is exceptional.48 Retrograde exten- sion of thrombus toward the suprahepatic veins, contralateral renal vein, and infrarenal IVC is com- mon once IVC invasion has led to caval obstruc- tion. Progressive obstruction of IVC promotes recruitment of collateral veins and limits the clini- cal manifestations of IVC involvement.68
IVC involvement must ideally be delineated preoperatively. Cavography can reveal collateral circulation but is usually not accurate enough to distinguish extrinsic caval compression from endo- luminal tumor extension or from the normal washout aspect of renal veins. Transesophageal echocardiography allows reliable visualization of tumoral extension into the cavoatrial junction or right atrium. CT scan and MRI are currently considered the most accurate modalities for assess- ment of ACC with IVC extension. 26,30,45,69,70 Both techniques provide direct evidence of tumor thrombus. MRI has an added ability to distinguish tumor thrombus from fibrinogenic thrombus.31 Involvement of the vein wall is usually diagnosed during surgical exploration only.
The optimal surgical approach of ACC with IVC extension depends on the size of the primary tumor, upper limit of intravenous extension, and need for associated procedures (nephrectomy, lymph node resection, hepatectomy for metastastic or contiguous intrahepatic spread). Control of IVC is an important consideration especially when CPB is to be performed. Laparotomy is sufficient for exposure of infrahepatic or retrohepatic caval extension. Laparotomy options include median and unilateral or bilateral subcostal. A combined thoracic and abdominal approach is the preferred technique for patients with retrohepatic and su- prahepatic caval involvement. In these cases, we use the bilateral subcostal approach with a vertical median extension ranging in length from a few centimeters to complete sternotomy. This route provides adequate exposure for all abdominal and thoracic procedures and for set-up of CPB.
The modality used for venous control depends on the location and extent of tumor involvement and the amount of collateral venous circulation (Fig 4). Cross clamping of the IVC is sufficient if the upper limit of tumor thrombus is located below the hepatic veins. HVE is the technique of choice for patients with extension into retro- or su- prahepatic but infradiaphragmatic IVC. Its toler- ance is generally good, provided fluid expansion
Adrenocortical carcinoma extending into the IVC
Evaluation of the upper limit of IVC extension: TEE, CT-Scan, MRI
Below hepatic veins (Extent A)
Retrohepatic IVC (Extent B) or Suprahepatic but infradiaphragmatic IVC
Supradiaphragmatic IVC (Extent C) and/or Right atrium
Cross-clamping
Hepatic vascular exclusion
Cardiopulmonary bypass
is performed before clamping.25 Although cross clamping of the intrapericardial IVC or partial clamping of the right atrium during HVE has been advocated for tumors extending into the lower edge of the cavoatrial junction,46 we con- sider that CPB should always be used for tumors extending to the cavoatrial junction or into the right atrium. CPB allows precise dissection by re- ducing bleeding and lowers the risk of cardiac ar- rest during caval cross clamping.25,55 Additionally, HCA provides a bloodless operating field and allows resection under visual control. In return, despite rewarming and heparin reversal, HCA followed by HVE to complete thrombus removal of retrohepatic IVC may lead to major coagulation disorders.
The results of our series confirm that throm- bectomy is effective for resection of tumor throm- bus not involving the venous wall. Cavotomy can be confined to the anterior wall of the IVC or initiated at the renal or adrenal vein level and prolonged upward as required by the thrombus extension. In case of involvement of the end of the IVC, vertical right atriotomy can be extended by cavotomy toward the level of the suprahepatic veins. Tumor thrombus associated with ACC has a jellylike, friable consistency similar to that of the
| Complete resection expected | Palliative resection expected | |
|---|---|---|
| Stage III Normal risk High risk | Surgery + adjuvant mitotane | Surgery + adjuvant mitotane therapy Discuss surgery + adjuvant mitotane therapy or mitotane therapy + anticancer chemotherapy |
| Surgery + therapy adjuvant mitotane therapy | ||
| Stage IV Normal risk | Surgery + adjuvant mitotane therapy | Surgery + adjuvant mitotane therapy |
| High risk | Discuss surgery + adjuvant mitotane therapy or mitotane therapy + anticancer chemotherapy | Mitotane therapy + anticancer chemotherapy |
primary tumor.37 Resection begins with dissection of minor adherences to the caval wall34 occurring at the level of the ostia of the right adrenal vein or left renal vein. Next, retrograde thrombectomy is performed by pulling the endoluminal mass down through the cavotomy. In cases of extension to the supradiaphragmatic IVC, anterograde throm- bectomy may be a safer method for clearing the cavosuprahepatic junction. Closure of cavotomy can be done by direct suture unless narrowing exceeds 50%.
Collateral circulation is well developed and makes prosthetic graft replacement unnecessary in most cases.46,71 However, when the venous wall is involved, complete resection of IVC may be required. The need to preserve venous outflow from the right kidney can justify caval replacement in selected cases.47,67,72 Despite reports describing successful caval replacement with prosthetic or venous grafts,66,73,74 we believe that this technique can be avoided in most cases.
Although vascular extension is generally consid- ered a sign of highly invasive malignancy, there is no conclusive evidence concerning the impact of IVC involvement in patients with ACC.59,62 Several
reports have shown that complete resection of the primary tumor and its venous extension can pro- long survival and improve quality of life.1,3,8,9 This may justify aggressive surgical treatment. Re- peat resection of recurrent or metastatic disease may improve survival rate and is recommended, when feasible.75 Most authors consider patients with IVC extension as having stage III ACC when metastases are absent. However, our results and those reported in the literature for such patients indicate that survival rate is poorer than the 25% 5 year-survival rate observed in patients with con- ventional stage III disease.4 We believe that, if sur- gery of the IVC allows complete resection of the primary tumor and its locoregional extension, in- volvement of the IVC should not be considered a contraindication for surgery. The question remains whether surgical treatment should be attempted in patients with stage IV metastatic disease and IVC extension, when life expectancy does not exceed 20% at 2 years.4 Reasons to advocate palliative re- section include palliation of tumoral symptoms, control of hormonal secretion for functioning ACC, and prevention of tumoral or cruoric pulmo- nary embolism. However, surgical treatment of such tumors is demanding and life threatening. “En bloc” complete resection of a huge friable tumor is rendered difficult by the presence of tumoral neovascularization and development of extensive collateral circulation, especially in pa- tients with secreting tumor and long-lasting expo- sure to steroids.76 In our review of the literature, 11 patients (17%, 11 of 65) died postoperatively or within 3 months after surgery. In case of meta- static disease and IVC extension, we believe that palliative surgery should be restricted to sympto- matic patients without severe comorbidity, in whom complete locoregional resection of primary ACC can be achieved (Table III).
The role of chemotherapy remains controversial. Partial response rates to mitotane treatment with no impact on survival rate have been reported.1,3,5,77 Significant side effects are frequent, and the sup- pressive effect on the unaffected adrenal gland, which requires lifelong steroid replacement ther- apy, should be taken into account.62 Because of the scarcity of cases, there is a lack of randomized, controlled trials concerning the efficacy of mitotane and still no consensus regarding adjuvant or pallia- tive medical therapy. Best results have been achieved by the combination of etoposide, doxorubicin, and cisplatin associated with mitotane with response rates ranging from 11% to 54% in phase II trials.78
Results in our series as well as data from the literature show that resection of ACC with
extension into the IVC is feasible. Careful preop- erative workup as well as mastery of deep vein surgery and CPB techniques are necessary to ensure the best chance of complete resection of the tumor and its extensions. This high-risk sur- gery is associated with a 10% to 15% mortality rate. Therefore, it should be avoided in patients with severe comorbidity or unresectable metastatic dis- ease. Long-term prognosis of ACC extending into the IVC remains poor because of the delay in diagnosis and lack of effective adjuvant treatment.
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