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8 Surgical Treatment of Adrenocortical Carcinoma with Caval Invasion

https://t.me/med1917

(median)

Overall survival

(median)

Disease-free

survival

(median)

6.1 ± 9.8 months

(median)

About 60 %

(5 years)

months

(median)

6 years (median)

(median)

157

13 % – 8 months

Postoperative

mortality

n = 2

Need for

prosthesis

Distal location of the

thrombus

Below the liver n = 2

Above the liver n = 7

Behind the liver n = 6

IVC

involvement

Number

patients

3 vein graft 13 % – 24 months

Extension to right

atrium n = 4

Subdiaphragmatic IVC

n = 6

Prehepatic IVC n = 21

SVC/right atrium n = 3

0 % 20 ± 7.7 months

n = 3

– – – 3 years

n = 39 (IVC

and large

% 8 months –

vessels)

Table 8.3 Summary of the main surgical series reporting IVC resection for ACC

Authors/years

Chiche/2006 105 14.3 %

Mihai/2012 35 –

Ohwada/2007 6 – –

Bednars/2014 53 – – – – About 20

Libé/2015 444 – – – – – 24 months

Turbendian/2010 57

Heddican/1997 3 – – No 30

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Conclusion

S. Gaujoux et al.

Involvement of the inferior vena cava by adrenocortical carcinoma is rare and associated with impaired oncologic outcome. Neoadjuvant chemotherapy is often poorly effective, while upfront complete surgical resection is potentially curative and should be preferred.

The surgery procedure mainly depends on the upper limit of intracaval extension:

– If the tumor thrombus is located below the suprahepatic veins, this representing

the most frequent clinical situation, cross-clamping of the IVC is sufﬁcient.

– If the tumor thrombus is located between the suprahepatic veins and the cavo-

atrial junction, hepatic vascular exclusion is the technique of choice, with intraor extrapericardial suprahepatic control.

– If the tumor thrombus is located above the cavo-atrial junction, hepatic vascular

exclusion with intrapericardial suprahepatic control can most of the time be done; otherwise, the use of cardiopulmonary bypass should be considered.

Key Points

– Caval invasion in patients with adrenocortical carcinoma is rare. – In our experience, the upper level of caval extension is best documented by the

combination of transesophageal echocardiography, CT scan, or angio-MRI.

– Most cases are represented by venous invasion and intracaval progression of a

tumor thrombus originating from the primary adrenal tumor.

– Direct invasion to the venous wall is often limited and can be treated by partial

wedge resection with direct closure or interposition of a patch.

– Caval resection with prosthetic replacement is indicated in less than 5 % of the

cases.

– The upper level of caval invasion can be located below, behind, or above the

hepatic vein conﬂuence, with or without right atrial extension.

– In most instances, caval thrombectomy can be performed by cross-clamping of

the IVC, conventional hepatic vascular exclusion, intrapericardial hepatic vascular exclusion, or cardiopulmonary bypass with hypothermic circulatory arrest.

Key References

– Chiche L et al (2006) Adrenocortical carcinoma extending into the inferior vena

cava: presentation of a 15-patient series and review of the literature. Surgery 139(1):15–27

– Mihai R et al (2012) Outcome of operation in patients with adrenocortical cancer

invading the inferior vena cava—a European Society of Endocrine Surgeons (ESES) survey. Langenbecks Arch Surg 397(2):225–231

– Turbendian HK et al (2010) Adrenocortical carcinoma: the inﬂuence of large

vessel extension. Surgery 148(6):1057–1064, discussion 1064

8 Surgical Treatment of Adrenocortical Carcinoma with Caval Invasion

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159

– Schteingart DE et al (2005) Management of patients with adrenal cancer: recom-

mendations of an international consensus conference. Endocr Relat Cancer 12(3):667–680

– Libe R et al (2015) Prognostic factors in stage III-IV adrenocortical carcinomas

(ACC): an European Network for the Study of Adrenal Tumor (ENSAT) study. Ann Oncol 26(10):2119–2125

– Margonis GA et al (2015) Adrenocortical carcinoma: impact of surgical margin

status on long-term outcomes. Ann Surg Oncol, Epub

References

1. Schteingart DE et al (2005) Management of patients with adrenal cancer: recommendations of

an international consensus conference. Endocr Relat Cancer 12(3):667–680

2. Wajchenberg BL et al (2000) Adrenocortical carcinoma: clinical and laboratory observations.

Cancer 88(4):711–736

3. Abiven G et al (2006) Clinical and biological features in the prognosis of adrenocortical can-

cer: poor outcome of cortisol-secreting tumors in a series of 202 consecutive patients. J Clin Endocrinol Metab 91(7):2650–2655

4. Icard P et al (2001) Adrenocortical carcinomas: surgical trends and results of a 253-patient series

from the French Association of Endocrine Surgeons study group. World J Surg 25(7):891–897

5. Icard P, Louvel A, Chapuis Y (1992) Survival rates and prognostic factors in adrenocortical

carcinoma. World J Surg 16(4):753–758

6. Libe R et al (2015) Prognostic factors in stage III-IV adrenocortical carcinomas (ACC): an

European Network for the Study of Adrenal Tumor (ENSAT) study. Ann Oncol 26(10):2119–2125

7. Ayala-Ramirez M et al (2013) Adrenocortical carcinoma: clinical outcomes and prognosis of

330 patients at a tertiary care center. Eur J Endocrinol 169(6):891–899

8. Margonis GA et al (2015) Adrenocortical carcinoma: impact of surgical margin status on long-

term outcomes. Ann Surg Oncol

9. Chiche L et al (2006) Adrenocortical carcinoma extending into the inferior vena cava: presen-

tation of a 15-patient series and review of the literature. Surgery 139(1):15–27

10. Mihai R et al (2012) Outcome of operation in patients with adrenocortical cancer invading the

inferior vena cava--a European Society of Endocrine Surgeons (ESES) survey. Langenbecks Arch Surg 397(2):225–231

11. Turbendian HK et al (2010) Adrenocortical carcinoma: the inﬂuence of large vessel extension.

Surgery 148(6):1057–1064, discussion 1064

12. Friedrich MG et al (1994) Adrenal carcinoma with intravenous extension into the tricuspid

valvular plane in a patient with patent foramen ovale. Eur Heart J 15(5):708–709

13. Carbonnel F et al (1988) Acute Budd-Chiari syndrome as ﬁrst manifestation of adrenocortical

carcinoma. J Clin Gastroenterol 10(4):441–444

14. Zini L, Porpiglia F, Fassnacht M (2011) Contemporary management of adrenocortical carci-

noma. Eur Urol 60(5):1055–1065

15. Low G, Sahi K (2012) Clinical and imaging overview of functional adrenal neoplasms. Int

Urol 19(8):697–708

16. Libe R, Fratticci A, Bertherat J (2007) Adrenocortical cancer: pathophysiology and clinical

management. Endocr Relat Cancer 14(1):13–28

17. Donatini G et al (2014) Long-term survival after adrenalectomy for stage I/II adrenocortical

carcinoma (ACC): a retrospective comparative cohort study of laparoscopic versus open approach. Ann Surg Oncol 21(1):284–291

18. Schramek P et al (1985) Adrenal cortical carcinoma: preoperative demonstration of right atrial

extension by sonography and computerized tomography. J Urol 133(2):260–262

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19. Pritchett TR et al (1987) Preoperative magnetic resonance imaging of vena caval tumor

thrombi: experience with 5 cases. J

20. Francis IR et al (1992) Integrated imaging of adrenal disease. Radiology 184(1):1–13

21. Smith SM et al (1989) Magnetic resonance imaging of adrenal cortical carcinoma. Urol Radiol

11(1):1–6

22. Decker RA, Kuehner ME (1991) Adrenocortical carcinoma. Am Surg 57(8):502–513

23. Bednarski BK et al (2014) Borderline resectable adrenal cortical carcinoma: a potential role

for preoperative chemotherapy. World J

24. Castleman B, Scully RE, McNeely BU (1972) Case records of the Massachusetts General

Hospital. Weekly clinicopathological exercises. Case 39–1972. N Engl J

25. Scully RE, Galdabini JJ, McNeely BU (1976) Case records of the Massachusetts General

Hospital. Weekly clinicopathological exercises. N Engl J Med 294(13):712–720

26. Shahian DM, Nieh PT, Libertino JA (1989) Resection of atriocaval adrenal carcinoma using

hypothermic circulatory arrest. Ann Thorac Surg 48(3):421–422

27. Moul JW, Hardy MR, McLeod DG (1991) Adrenal cortical carcinoma with vena cava tumor

thrombus requiring cardiopulmonary bypass for resection. Urology 38(2):179–183

28. Cheung PS, Thompson NW (1989) Right atrial extension of adrenocortical carcinoma. Surgical

management using hypothermia and cardiopulmonary bypass. Cancer 64(4):812–815

29. Huguet C et al (1994) Neoplastic thrombosis of the inferior vena cava involving the right

atrium caused by adrenal cortical carcinoma. A new indication for vascular exclusion of the liver. Ann Chir 48(4):364–369

30. Bower TC et al (1993) Vena cava replacement for malignant disease: is there a role? Ann Vasc

Surg 7(1):51–62

31. Gloviczki P et al (1990) Reconstruction of the vena cava and of its primary tributaries: a pre-

liminary report. J Vasc Surg 11(3):373–381

32. Wang Q et al (2012) Leiomyosarcoma of the inferior vena cava level II involvement: curative

resection and reconstruction of renal veins. World J Surg Oncol 10:120

33. Araujo RL et al (2014) End-to-end renal vein anastomosis to preserve renal venous drainage

following inferior vena cava radical resection due to leiomyosarcoma. Ann Vasc Surg 28(4):1048–1051

34. Le Treut YP et al (2013) Transdiaphragmatic extrapericardial approach of the inferior vena

cava. J Am Coll Surg 217(5):e41–e43

35. Smith BM et al (1984) Suprarenal vena caval occlusion. Principles of operative management.

Ann Surg 199(6):656–668

36. Patil MB et al (2014) Level III-IV inferior vena caval thrombectomy without cardiopulmonary

bypass: long-term experience with intrapericardial control. J Urol 192(3):682–688

37. Hedican SP, Marshall FF (1997) Adrenocortical carcinoma with intracaval extension. J Urol

158(6):2056–2061

Urol 138(5):1220–1222

Surg 38(6):1318–1327

Med 287(13):656–663

Malignancy with Cavoatrial Extension

https://t.me/med1917

Jean-Marc Alsac, Paul Achouh, Eleonora Du Puymontbrun, Alain

Bel, Jerome Jouan, Suzanna Salvi, Julia Pouly,

Jean-Noël Fabiani

and

9.1 Introduction

Abdominal tumors with involvement of the inferior vena cava (IVC) are most frequently of renal origin or sarcomas [1]. Ten percent of renal tumors invade the IVC, and 1 % extend up to the right atrium [2, 3]. Nevertheless, extensive caval inﬁltration or extension to the heart is uncommon. This latter situation is challenging as surgical difﬁculties and postoperative complications rise along with the level of extension of the thrombus in the IVC and the involvement of surrounding structures [4, 5]. Even in the presence of local invasion or metastasis, surgical resection is the only treatment shown to improve survival in these patients [5, 6]. The use of cardiopulmonary bypass (CPB), for tumors extending to the level of the hepatic veins or into the atrium, is highly recommended [5, 7]. Several series report the use of CPB with deep hypothermia and circulatory arrest (DHCA) [3,

7], but these procedures are associated with signiﬁcant mortality. For renal cell

carcinoma with cavoatrial extension, a recent multi-institutional study reported an

8.3 % operative mortality with the use of DHCA [3]. Despite the fact that deep

hypothermia provides organ protection, circulatory arrest is associated with a higher risk of neurologic complications and ischemia—reperfusion injury [8]. We reported our experience with the use of CPB and deep hypothermia without circulatory arrest in the surgical treatment of abdominal tumors with IVC and right atrial involvement [9].

J.-M. Alsac, MD, PhD • P. Achouh, MD, PhD • E. Du Puymontbrun, MD • A. Bel, MD J. Jouan, MD • S. Salvi, MD • J. Pouly, MD • J.-N. Fabiani, MD ( Service de Chirurgie Cardiaque et Vasculaire, Hôpital Européen Georges Pompidou, AP-HP, Faculté de Médecine René Descartes, Université Paris 5, Paris, France e-mail: jean-noel.fabiani@egp.aphp.fr

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9.2 Preoperative Staging

The staging should include thoracoabdominal computed tomography scan and magnetic resonance angiography to assess tumor extension and rule out metastasis. The upper extent of the tumor thrombus is deﬁned in accordance with the classiﬁcation of Neves and Zincke [10], which encompasses four stages. Stage 1 includes tumors with thrombus extension less than 2 cm in the IVC. Stage 2 is for thrombus extension below the hepatic veins. Intrahepatic IVC thrombus extension that remains below the diaphragm corresponds to stage 3. Thrombus extension above the diaphragm is stage 4. In case of cardiac extension of the tumoral thrombus, the tumor may cross the tricuspid valve. Acute Budd-Chiari syndrome can be seen preoperatively in case of severe hepatic vein obstruction.

9.3 Surgical Technique

Under general anesthesia, the right common femoral vein is exposed through a groin incision and prepared for cannulation. A complete median sternotomy is performed. Depending on the location of the primary tumor, the sternotomy should be extended through a right subcostal incision for right renal, hepatic, and primary IVC tumors. Bilateral subcostal incision or median laparotomy should be used for left renal and left adrenal primary tumors. The pericardium is opened, and the ascending aorta is cannulated. The superior vena cava and common femoral vein are cannulated to ensure venous drainage of the upper half and lower half of the body. Mobilization of the right colon is followed by a Kocher maneuver to expose the IVC and the renal veins. The falciform ligament and the right triangular ligament are incised to allow a right hepatic lobe mobilization and exposure of the suprarenal and retrohepatic vena cava. An anteroposterior phrenotomy is achieved, widely exposing the hepatic veins and the cavoatrial junction.

Concomitant to the beginning of tumor resection and vena cava dissection, CPB

is started and systemic cooling initiated until cessation of all electrical brain activity. This would usually be achieved at an esophageal temperature of 18–20 °C. The decrease and then cessation of electrical brain activity is assessed by electroencephalography. Once the electroencephalogram is ﬂat, CPB ﬂow is decreased from 1 to 1.5 phrenic, and adrenal veins, facilitating dissection, tumoral resection, and atriohepatic conﬂuent reconstruction.

Then, under deep hypothermia and low CPB ﬂow, the IVC and right atrium are opened to assess thrombus extension (Figs. 9.1 and 9.2) and to consider the patency of the hepatic veins (Fig. 9.3). The right atrium is incised parallel to the right atrioventricular sulcus. When the IVC is invaded, an en bloc resection of the inﬁltrated part with removal of the tumoral thrombus should be carried out, respecting carcinoid margins. In the case of preoperative Budd-Chiari syndrome, the hepatic veins are thrombectomized. Small secondary veins are ligated, and the major hepatic veins

L/min. This would decrease the venous return through hepatic, lumbar,

In case of renal or adrenal cancer, the primary tumor would be ﬁrst removed.

9 Malignancy with Cavoatrial Extension

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Fig. 9.1 Longitudinal opening of right atrium and inferior vena cava allowing exposure of the thrombus and the origin of the hepatic veins

Fig. 9.2 Extraction of the tumoral thrombus from the hepatic veins and the right heart, and resection of the infrahepatic inferior vena cava (IVC)

163

Fig. 9.3 Surgical ﬁeld after thrombus removal, with veriﬁcation of the patency of the hepatic veins

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Fig. 9.4 Atriohepatic conﬂuent reconstruction with direct anastomosis of the hepatic veins in the right atrium, using a pericardium patch

J.-M. Alsac et al.

are reimplanted directly into the right atrium, using a bovine pericardial patch to offset tissue loss (Fig. 9.4), as initially described by Pasic and associates [11]. If IVC is occluded preoperatively (conﬁrmed by preoperative imaging and by operative ﬁndings), no vena cava reconstruction (bypass) should be performed. The IVC is usually interrupted just distal to the remaining renal veins. The venous drainage of the lower part of the body and of the renal veins will be achieved through the cavoazygos collateral system.

After completion of hepatic vein reconstruction and anastomosis to the right

atrium, CPB normal ﬂow can be restored and rewarming started up to a central temperature (bladder or rectal temperature) of 36.5 °C. Then CPB is stopped, cannulas removed, heparin neutralized, and careful hemostasis performed in the thoracic and abdominal cavities.

9.4 Postoperative Management

Postoperatively, patients are placed in light Trendelenburg position to improve venous drainage of the inferior part of the body after interruption of the IVC. Compression stockings can be used to avoid lower limb edema. Patients are also started on intravenous anticoagulation as soon as bleeding is controlled and then switched to oral anticoagulation for at least a year, to prevent extensive thrombosis of the iliac and lower limb venous system. A control computed tomography angiography scan is recommended before hospital discharge, to control the patency of the atriohepatic reconstruction.

9.5 Discussion

In such complex reconstructions of the atriohepatic outﬂow, this technique seems safe and allows longer surgical time than circulatory arrest. While ensuring organ protection by a combination of both hypothermia and continuous perfusion, it is

9 Malignancy with Cavoatrial Extension

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165

associated with a lower risk of neurologic complications. Several other techniques have already been reported in the literature. All these techniques of resection of the IVC and atrial malignancy extension depend on the cephalad extension of the tumor and are independent from the nature of the tumor.

A recent literature review published by Lawindy and coworkers [5] provides

guidelines on the surgical management of cavoatrial extension of renal cell carcinomas. For stages 1 (renal) and 2 (retrohepatic) thrombi, a classic abdominal approach without the use of CPB is recommended, with control of the IVC proximal and distal to the tumor. For high-level tumors (stages 3 and 4), a median sternotomy is often required to obtain vascular control distal to the thrombus. Potential complications related to these procedures, such as major bleeding and hypotension, are important concerns. This review clearly states that the use of CPB can easily circumvent such major adverse events [5]. The use of CPB is, nowadays, an essential adjunct for the management of these diseases. The surgical management of IVC leiomyosarcoma is relatively similar, but as this tumor is a rare entity, there are no consensus guidelines. To date, only 300 such cases have been reported in the literature [12].

According to multiple reports, there are two pivotal key points to guarantee a

successful surgical procedure. The ﬁrst key point is the quality of exposure of the operating ﬁeld, which is essential to perform a complete resection of the tumoral tissues. Any signiﬁcant back-bleeding from the hepatic and lumbar veins often compromises this exposure. Many authors highlighted that a reduced view of the operating ﬁeld was responsible for incomplete tumor resection, higher risk of warm hepatic or renal ischemia, pulmonary embolism, and acute tubular necrosis [13–16]. The second key point is precise control of any potential major bleeding from the liver venous circulation with the use of CPB [4, 13].

In a report by Ciancio and colleagues [17], 12 patients were surgically treated

without sternotomy or CPB. All 12 patients had thrombus, which did not extend deeply in the right atrium, and no tumoral invasion of the retrohepatic IVC. Thus, the tumor could be “milked” out of the right atrium in these patients. In some of these patients, blood inﬂow to the liver had to be interrupted to achieve a bloodless ﬁeld and to allow opening of the retrohepatic IVC.

Even in these last cases, no resection and subsequent reconstruction of the retrohepatic IVC had to be done, so hepatic cross-clamp time was short. Skinners and coworkers [18] described intraatrial thrombus retrieval using CPB, in combination with hepatic vascular exclusion. This technique allows a cavotomy with a remarkable reduction of bleeding from the hepatic veins. Nevertheless, in some cases of chronic IVC obstruction, collaterals such as phrenic veins, lumbars, short hepatic, or adrenal veins become major drainage pathways, bringing unexpected back-bleeding [13]. In their series, the authors reported a high rate (41–60 %) of postoperative complications, including transient hyperbilirubinemia and renal failure [18].

The technique most frequently encountered in the literature is the use of CPB with DHCA [4, 5, 7]. The bloodless ﬁeld obtained allows an excellent visualization of the tumor and decreases the risk of cellular spreading, incomplete tumor excision, pulmonary embolism, or warm hepatic or renal ischemia. Nevertheless, there are several disadvantages of DHCA, such as end-organ dysfunction, ischemic injury, and ischemia–reperfusion injury. Furthermore, the duration of DHCA is

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limited, with a safe duration of circulatory arrest of 30 min at 18 °C [8] according to some reports. Knowing that complete tumor excision with respect to carcinoid margins remains the principal issue qualifying the success of the operation and long- term survival of patients [6], achieving this can be technically challenging and time-consuming, especially in patients with invasion of surrounding structures.

Cardiopulmonary bypass with deep hypothermic low ﬂow combines, in our experience, the protective effects of hypothermia associated with the positive effect of a continuous low-ﬂow blood perfusion. This allows a longer safe surgery time with a lower risk of organ ischemia. Deep hypothermic low ﬂow (1–1.5 L/min, which can be modulated according to the venous backﬂow) provides a nearly bloodless ﬁeld, considerably reducing back-bleeding not only from the hepatic veins but also from the lumbar, adrenal, and short hepatic veins and thus allowing an excellent visualization of the tumor. This technique avoids hepatic vascular exclusion, which requires dissection of hepatic vessels and induces ischemic liver injury owing to cross-clamping. Continuous CPB outﬂow decreases the risk of cerebral ischemia and stroke. We believe that this technique can facilitate surgical management of these patients, providing a bloodless ﬁeld with a high level of organ protection. In all cases, a multidisciplinary approach is mandatory for these procedures.

Cardiopulmonary bypass with deep hypothermic low ﬂow needs to be considered as a surgical option in patients with abdominal and retroperitoneal tumors invading the IVC and extending to the right atrium, when there is a need for extensive resection of the IVC and reconstruction of the hepatic vein conﬂuence. This technique is reliable and allows a longer safe operative time and organ protection, often necessary to obtain complete excision of the tumor, associated with an excellent view of the surgical ﬁeld.

References

1. Quinones-Baldrich W, Alktaiﬁ A, Eilber F, Eilber F (2012) Inferior vena cava resection and

reconstruction for retroperitoneal tumor excision. J Vasc Surg 55:1386–1393

2. Chiappini B, Savini C, Marinelli G et al (2002) Cavoatrial tumor thrombus: single-stage surgi-

cal approach with profound hypothermia and circulatory arrest, including a review of the literature. J

3. Shuch B, Crispen PL, Leibovich BC et al (2011) Cardiopulmonary bypass and renal cell car-

cinoma with level IV tumour thrombus: can deep hypothermic circulatory arrest limit perioperative mortality? BJU Int 107:724–728

4. Dedeilias P, Koletsis E, Rousakis AG et al (2009) Deep hypothermia and circulatory arrest in

the surgical management of renal tumors with cavoatrial extension. J Card Surg 24:617–623

5. Lawindy SM, Kurian T, Kim T et al (2012) Important surgical considerations in the manage-

ment of renal cell carcinoma (RCC) with inferior vena cava (IVC) tumour thrombus. BJU Int 110:926–939

6. Kuehnl A, Schmidt M, Hornung HM, Graser A, Jauch KW, Kopp R (2007) Resection of malig-

nant tumors invading the vena cava: perioperative complications and long-term follow-up. J Vasc Surg 46:533–540

Thorac Cardiovasc Surg 124:684–688

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