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Removal of hepatocellular carcinoma extending in the right atrium without extracorporal bypass
SURGEON AT WORK
Removal of Hepatocellular Carcinoma Extending in the Right Atrium without Extracorporal Bypass Martine Georgen, MD, Jean-Marc Regimbeau, MD, Reza Kianmanesh, MD, Jean Marty, MD, Olivier Farges, MD, PhD, Jacques Belghiti, MD the liver and en bloc retraction of the tumor and the thrombus out of the RA; 3) after application of a vascular clamp on the suprahepatic portion of the IVC above the thrombus, a routine hepatic vascular exclusion can be performed to remove the tumor and the thrombus.
Invasion of the inferior vena cava (IVC) and the right atrium by hepatocellular carcinoma is a rare but lifethreatening condition. To avoid embolism and sudden death, the aggressive resection of both the tumor and its thrombus represents the only treatment modality that can offer hope for better survival of these patients. All the reported resection cases include the use of cardiopulmonary bypasses. The original thoracoabdominal finger-assisted approach described here is based on complete mobilization of the liver, which allows en bloc retraction of the tumor and the thrombus out of the right atrium and hepatic vascular exclusion that avoids the need for extracorporal bypass. Invasion of the IVC and the right atrium (RA) by hepatocellular carcinoma (HCC) concerns less than 2% of the patients with HCC,1,2 but represents a lifethreatening entity. The major causes of death are sudden pulmonary embolism of the thrombus or acute obstruction of the tricuspid valve or both.3,4 Resection can provide relatively longterm survival in this particular clinical situation, up to 2 years,5 but all the described surgical procedures, aimed to remove the thrombus and the tumor, require either an extracorporal circulation or venovenous bypasses.6,7 Both procedures are technically complex and present their own morbidity. We describe an original finger-assisted thoracoabdominal approach for resection of HCC with thrombus extending into the RA, assisted by transesophageal echocardiography (TEE), that avoids the need for extracorporal bypass. There are three prerequisites for this procedure: 1) there are no adhesions to the venous wall of macroscopic thrombus in patients with HCC;8 2) complete mobilization of the liver allows caudal retraction of
CASE A 22-year-old woman (AgHBS positive) was operated on in September 1995 for a HCC revealed during pregnancy and had a left hepatectomy. Postoperative course was uneventful. Pathologic examination of the specimen revealed a 6 cm in diameter HCC, moderately differentiated, with capsule invasion, microvascular thrombus, and a disease-free margin developed on a fibrotic nontumorous liver. After 4 years of uneventful followup (September 1999), she presented with asthenia and weight loss. Liver function tests were normal except for a moderate cytolysis (alanine transaminases 6N, aspartate transaminases 3N). Abdominal ultrasonography and computed tomography revealed a tumoral thrombus (28 ⫻ 17 mm) in the IVC and the RA, and a 3-cm tumor located in the upper part of segment VII of the liver. To prevent sudden migration of the thrombus, a surgical resection was performed. Surgical procedure
The patient was placed in a left lateral position. A right anterolateral thoracotomy in the 7th intercostal space with an extension to the abdomen and dissection of the diaphragm was performed to provide good exposure of the retro- and suprahepatic IVC and the RA. Peroperative liver ultrasonographic examination confirmed the presence of a single intrahepatic lesion. TEE was used during the whole procedure to detect the part of the tumor flowing into the pulmonary artery or occluding the tricuspid valve. The liver was completely mobilized by dividing the falciform, right triangular ligaments, and all the retrohepatic IVC. Exposition of the retrohepatic IVC required control of the right adrenal vein, caudate lobe veins, and
No competing interests declared.
Received February 27, 2002; Revised July 16, 2002; Accepted July 16, 2002. From the Department of Hepatopancreatic and Biliary Surgery (Georgen, Regimbeau, Kianmanesh, Farges, Belghiti), Clichy, France and the Department of Anesthesia-Intensive Care (Marty), Hospital Beaujon, University of Paris, Clichy, France. Correspondence and reprints to: Pr Jacques Belghiti, Department of Surgery, Beaujon Hospital, 100 boulevard du Ge´ne´ral Leclerc, 92118 Clichy, France.
© 2002 by the American College of Surgeons Published by Elsevier Science Inc.
892
ISSN 1072-7515/02/$21.00 PII S1072-7515(02)01497-7
Vol. 195, No. 6, December 2002
Figure 1. Complete mobilization of the liver allowed caudal retraction of the liver and “en bloc” retraction of the tumor and the thrombus out of the right atrium.
accessory inferior right hepatic veins. This complete mobilization of the liver allowed retraction of the liver caudally in the abdomen and en bloc retraction of the tumor and the thrombus out of the RA (Figure 1): TEE confirmed mobility of the thrombus. The IVC above and below the liver and the hepatoduodenal ligament had been previously encircled by a tourniquet. A finger-assisted palpation of the tumor through the invaginated wall of the RA under TEE monitoring (Figure 2) (concomitant retraction of the liver) allowed us to push down the thrombus below the suprahepatic IVC tourniquet (Figure 2). Previously, vascular clamps were applied to the hepatoduodenal ligament and infrahepatic IVC. Hepatic vascular exclusion was then started. Total vascular clamping has been well tolerated. A short venotomy in a longitudinal fashion of the atrial part of the IVC was performed. Then, with Babcock forceps, the thrombus was removed and exploration of the lumen of the right hepatic vein showed no remnant thrombus, allowing removal of the total vascular exclusion after 15 minutes (blood loss was 650 ml).
Georgen et al
Removal of Hepatocellular Carcinoma
893
Figure 2. A finger-assisted palpation of the tumor through the invaginated wall of the right atrium associated with a concomitant retraction of the liver. The thrombus is below the suprahepatic IVC tourniquet. Transesophageal echocardiography monitoring showing the surgeon’s finger in the right atrium and the thrombus (cartouche).
Then, a classic limited hepatic resection was performed to remove the liver tumor. The postoperative course was uneventful (an intensive care unit stay of 12 days) and the patient was discharged on the 26th day after surgery. The patient led an active life for 23 months after operation without any evidence of tumor recurrence. Then she experienced both pulmonary and liver recurrence and she died 30 months after the operation. Since then, we have performed this procedure in three patients, with no need for extracorporal bypass. DISCUSSION Results of surgical treatment of HCC have improved considerably in terms of safety and applicability in recent years. But tumors extending into the IVC have a poor prognosis, and the aggressive resection of both the tumor and its thrombus, to avoid embolism and sudden death, represents the only treatment modality that might offer hope for better survival of these patients.
894
Georgen et al
Removal of Hepatocellular Carcinoma
This procedure, because of the extension of the disease (as shown in the reported case), could not be performed in a curative attempt. All the reported resection cases include the use of cardiopulmonary bypasses,6,7,9 but these procedures have their own morbidity, mainly from the technical complexity of these procedures. After cardiopulmonary bypass, uncontrollable bleeding can occur, especially in cirrhotic patients. In addition, there are possible complications, such as adult respiratory distress syndrome and intravascular coagulation.10 To reduce the risk of massive bleeding and major vascular injury, other procedures have been suggested, such as veno-venous bypass, use of concomitant hypothermia, or total circulatory arrest with exsanguinations.11 The rationale for this technique is that there are no or minimal adhesions to the venous wall of macroscopic thrombus in case of HCC.8,12 So, the originality of this finger-assisted procedure lies in the fact that after complete mobilization and caudal retraction of the liver, it results in a classic hepatic vascular exclusion of the liver. Consequently, there’s no point in using cardiopulmonary bypasses. Hepatic vascular exclusion of the liver has been well investigated for lesions involving cavohepatic intersection, and is not tolerated in less than 15% of the patients.13,14 The most important technical point of this technique is the need of a total mobilization of the liver (facilitated by the right thoracophrenolaparotomy), including the caudate lobe for better traction of the liver and the thrombus down to the suprahepatic IVC. In conclusion, we suggest including this finger-assisted approach among the available surgical tools of the surgeon for resection of selected liver tumors. Author Contributions
Study conception and design: Belghiti Acquisition of data: Georgen, Regimbeau Analysis and interpretation of data: Georgen, Marty, Kianmanesh Drafting of manuscript: Georgen Critical revision: Farges
J Am Coll Surg
Supervision: Belghiti REFERENCES 1. Edmonson HA, Steiner PE. Primary carcinoma of the liver: study of 100 cases among 48,900 necropsies. Cancer 1954;7: 462–503. 2. Kanematsu M, Imaeda T, Minowa H, et al. Hepatocellular carcinoma with tumor thrombus in the inferior vena cava and right atrium. Abdom Imaging 1994;19:313–316. 3. Chomette G, Auriol M, Sevestre C, Acar J. Metastatic pulmonary emboli: clinical types and incidence. Ann Med Interne 1980;131:217–221. 4. Koskinas J, Betrosian A, Kafiri G, et al. Combined hepatocellular-cholangiocarcinoma presented with massive pulmonary embolism. Hepatogastroenterology 2000;47:1125– 1128. 5. Fujisaki M, Kurihara E, Kikuchi K, et al. Hepatocellular carcinoma with tumor thrombus extending into the right atrium: report of a successful resection with the use of cardiopulmonary bypass. Surgery 1991;109:214–219. 6. Iemura J, Aoshima M, Ishigami N, et al. Surgery for hepatocellular carcinoma with tumor thrombus in the right atrium. Hepatogastroenterology 1997;44:824–825. 7. Yogita S, Tashiro S, Harada M, et al. Hepatocellular carcinoma with extension into the right atrium: report of a successful liver resection by hepatic vascular exclusion using cardiopulmonary bypass. J Med Invest 2000;47:155–160. 8. Kojiro M, Nakashima T. Pathology of hepatocellular carcinoma. In: Okuda K, Kamal GI, eds. Neoplasms of the liver. Tokyo: Springer-Verlag; 1987:81–104. 9. Togo S, Shimada H, Tanaka K, et al. Management of malignant tumor with intracaval extension by selective clamping of IVC. Hepatogastroenterology 1996;43:1165–1171. 10. Fazel S, Everson EA, Stitt LW, et al. Predictors of general surgical complications after heart transplantation. J Am Coll Surg 2001; 193:52–59. 11. Wu CC, Hseih S, Ho WM, et al. Surgical treatment for recurrent hepatocellular carcinoma with tumor thrombi in right atrium: using cardiopulmonary bypass and deep hypothermic circulatory arrest. J Surg Oncol 2000;74:227–2231. 12. Clayman RV Jr, Gonzalez R, Fraley EE. Renal cancer invading the inferior vena cava: clinical review and anatomical approach. J Urol 1980;123:157–163. 13. Delva E, Barberousse JP, Nordlinger B, et al. Hemodynamic and biochemical monitoring during major liver resection with use of hepatic vascular exclusion. Surgery 1984;95:309–318. 14. Belghiti J, Noun R, Zante E, et al. Portal triad clamping or hepatic vascular exclusion for major liver resection. A controlled study. Ann Surg 1996;224:155–161.
Removal of Hepatocellular Carcinoma Extending in the Right Atrium without Extracorporal Bypass Martine Georgen, MD, Jean-Marc Regimbeau, MD, Reza Kianmanesh, MD, Jean Marty, MD, Olivier Farges, MD, PhD, Jacques Belghiti, MD the liver and en bloc retraction of the tumor and the thrombus out of the RA; 3) after application of a vascular clamp on the suprahepatic portion of the IVC above the thrombus, a routine hepatic vascular exclusion can be performed to remove the tumor and the thrombus.
Invasion of the inferior vena cava (IVC) and the right atrium by hepatocellular carcinoma is a rare but lifethreatening condition. To avoid embolism and sudden death, the aggressive resection of both the tumor and its thrombus represents the only treatment modality that can offer hope for better survival of these patients. All the reported resection cases include the use of cardiopulmonary bypasses. The original thoracoabdominal finger-assisted approach described here is based on complete mobilization of the liver, which allows en bloc retraction of the tumor and the thrombus out of the right atrium and hepatic vascular exclusion that avoids the need for extracorporal bypass. Invasion of the IVC and the right atrium (RA) by hepatocellular carcinoma (HCC) concerns less than 2% of the patients with HCC,1,2 but represents a lifethreatening entity. The major causes of death are sudden pulmonary embolism of the thrombus or acute obstruction of the tricuspid valve or both.3,4 Resection can provide relatively longterm survival in this particular clinical situation, up to 2 years,5 but all the described surgical procedures, aimed to remove the thrombus and the tumor, require either an extracorporal circulation or venovenous bypasses.6,7 Both procedures are technically complex and present their own morbidity. We describe an original finger-assisted thoracoabdominal approach for resection of HCC with thrombus extending into the RA, assisted by transesophageal echocardiography (TEE), that avoids the need for extracorporal bypass. There are three prerequisites for this procedure: 1) there are no adhesions to the venous wall of macroscopic thrombus in patients with HCC;8 2) complete mobilization of the liver allows caudal retraction of
CASE A 22-year-old woman (AgHBS positive) was operated on in September 1995 for a HCC revealed during pregnancy and had a left hepatectomy. Postoperative course was uneventful. Pathologic examination of the specimen revealed a 6 cm in diameter HCC, moderately differentiated, with capsule invasion, microvascular thrombus, and a disease-free margin developed on a fibrotic nontumorous liver. After 4 years of uneventful followup (September 1999), she presented with asthenia and weight loss. Liver function tests were normal except for a moderate cytolysis (alanine transaminases 6N, aspartate transaminases 3N). Abdominal ultrasonography and computed tomography revealed a tumoral thrombus (28 ⫻ 17 mm) in the IVC and the RA, and a 3-cm tumor located in the upper part of segment VII of the liver. To prevent sudden migration of the thrombus, a surgical resection was performed. Surgical procedure
The patient was placed in a left lateral position. A right anterolateral thoracotomy in the 7th intercostal space with an extension to the abdomen and dissection of the diaphragm was performed to provide good exposure of the retro- and suprahepatic IVC and the RA. Peroperative liver ultrasonographic examination confirmed the presence of a single intrahepatic lesion. TEE was used during the whole procedure to detect the part of the tumor flowing into the pulmonary artery or occluding the tricuspid valve. The liver was completely mobilized by dividing the falciform, right triangular ligaments, and all the retrohepatic IVC. Exposition of the retrohepatic IVC required control of the right adrenal vein, caudate lobe veins, and
No competing interests declared.
Received February 27, 2002; Revised July 16, 2002; Accepted July 16, 2002. From the Department of Hepatopancreatic and Biliary Surgery (Georgen, Regimbeau, Kianmanesh, Farges, Belghiti), Clichy, France and the Department of Anesthesia-Intensive Care (Marty), Hospital Beaujon, University of Paris, Clichy, France. Correspondence and reprints to: Pr Jacques Belghiti, Department of Surgery, Beaujon Hospital, 100 boulevard du Ge´ne´ral Leclerc, 92118 Clichy, France.
© 2002 by the American College of Surgeons Published by Elsevier Science Inc.
892
ISSN 1072-7515/02/$21.00 PII S1072-7515(02)01497-7
Vol. 195, No. 6, December 2002
Figure 1. Complete mobilization of the liver allowed caudal retraction of the liver and “en bloc” retraction of the tumor and the thrombus out of the right atrium.
accessory inferior right hepatic veins. This complete mobilization of the liver allowed retraction of the liver caudally in the abdomen and en bloc retraction of the tumor and the thrombus out of the RA (Figure 1): TEE confirmed mobility of the thrombus. The IVC above and below the liver and the hepatoduodenal ligament had been previously encircled by a tourniquet. A finger-assisted palpation of the tumor through the invaginated wall of the RA under TEE monitoring (Figure 2) (concomitant retraction of the liver) allowed us to push down the thrombus below the suprahepatic IVC tourniquet (Figure 2). Previously, vascular clamps were applied to the hepatoduodenal ligament and infrahepatic IVC. Hepatic vascular exclusion was then started. Total vascular clamping has been well tolerated. A short venotomy in a longitudinal fashion of the atrial part of the IVC was performed. Then, with Babcock forceps, the thrombus was removed and exploration of the lumen of the right hepatic vein showed no remnant thrombus, allowing removal of the total vascular exclusion after 15 minutes (blood loss was 650 ml).
Georgen et al
Removal of Hepatocellular Carcinoma
893
Figure 2. A finger-assisted palpation of the tumor through the invaginated wall of the right atrium associated with a concomitant retraction of the liver. The thrombus is below the suprahepatic IVC tourniquet. Transesophageal echocardiography monitoring showing the surgeon’s finger in the right atrium and the thrombus (cartouche).
Then, a classic limited hepatic resection was performed to remove the liver tumor. The postoperative course was uneventful (an intensive care unit stay of 12 days) and the patient was discharged on the 26th day after surgery. The patient led an active life for 23 months after operation without any evidence of tumor recurrence. Then she experienced both pulmonary and liver recurrence and she died 30 months after the operation. Since then, we have performed this procedure in three patients, with no need for extracorporal bypass. DISCUSSION Results of surgical treatment of HCC have improved considerably in terms of safety and applicability in recent years. But tumors extending into the IVC have a poor prognosis, and the aggressive resection of both the tumor and its thrombus, to avoid embolism and sudden death, represents the only treatment modality that might offer hope for better survival of these patients.
894
Georgen et al
Removal of Hepatocellular Carcinoma
This procedure, because of the extension of the disease (as shown in the reported case), could not be performed in a curative attempt. All the reported resection cases include the use of cardiopulmonary bypasses,6,7,9 but these procedures have their own morbidity, mainly from the technical complexity of these procedures. After cardiopulmonary bypass, uncontrollable bleeding can occur, especially in cirrhotic patients. In addition, there are possible complications, such as adult respiratory distress syndrome and intravascular coagulation.10 To reduce the risk of massive bleeding and major vascular injury, other procedures have been suggested, such as veno-venous bypass, use of concomitant hypothermia, or total circulatory arrest with exsanguinations.11 The rationale for this technique is that there are no or minimal adhesions to the venous wall of macroscopic thrombus in case of HCC.8,12 So, the originality of this finger-assisted procedure lies in the fact that after complete mobilization and caudal retraction of the liver, it results in a classic hepatic vascular exclusion of the liver. Consequently, there’s no point in using cardiopulmonary bypasses. Hepatic vascular exclusion of the liver has been well investigated for lesions involving cavohepatic intersection, and is not tolerated in less than 15% of the patients.13,14 The most important technical point of this technique is the need of a total mobilization of the liver (facilitated by the right thoracophrenolaparotomy), including the caudate lobe for better traction of the liver and the thrombus down to the suprahepatic IVC. In conclusion, we suggest including this finger-assisted approach among the available surgical tools of the surgeon for resection of selected liver tumors. Author Contributions
Study conception and design: Belghiti Acquisition of data: Georgen, Regimbeau Analysis and interpretation of data: Georgen, Marty, Kianmanesh Drafting of manuscript: Georgen Critical revision: Farges
J Am Coll Surg
Supervision: Belghiti REFERENCES 1. Edmonson HA, Steiner PE. Primary carcinoma of the liver: study of 100 cases among 48,900 necropsies. Cancer 1954;7: 462–503. 2. Kanematsu M, Imaeda T, Minowa H, et al. Hepatocellular carcinoma with tumor thrombus in the inferior vena cava and right atrium. Abdom Imaging 1994;19:313–316. 3. Chomette G, Auriol M, Sevestre C, Acar J. Metastatic pulmonary emboli: clinical types and incidence. Ann Med Interne 1980;131:217–221. 4. Koskinas J, Betrosian A, Kafiri G, et al. Combined hepatocellular-cholangiocarcinoma presented with massive pulmonary embolism. Hepatogastroenterology 2000;47:1125– 1128. 5. Fujisaki M, Kurihara E, Kikuchi K, et al. Hepatocellular carcinoma with tumor thrombus extending into the right atrium: report of a successful resection with the use of cardiopulmonary bypass. Surgery 1991;109:214–219. 6. Iemura J, Aoshima M, Ishigami N, et al. Surgery for hepatocellular carcinoma with tumor thrombus in the right atrium. Hepatogastroenterology 1997;44:824–825. 7. Yogita S, Tashiro S, Harada M, et al. Hepatocellular carcinoma with extension into the right atrium: report of a successful liver resection by hepatic vascular exclusion using cardiopulmonary bypass. J Med Invest 2000;47:155–160. 8. Kojiro M, Nakashima T. Pathology of hepatocellular carcinoma. In: Okuda K, Kamal GI, eds. Neoplasms of the liver. Tokyo: Springer-Verlag; 1987:81–104. 9. Togo S, Shimada H, Tanaka K, et al. Management of malignant tumor with intracaval extension by selective clamping of IVC. Hepatogastroenterology 1996;43:1165–1171. 10. Fazel S, Everson EA, Stitt LW, et al. Predictors of general surgical complications after heart transplantation. J Am Coll Surg 2001; 193:52–59. 11. Wu CC, Hseih S, Ho WM, et al. Surgical treatment for recurrent hepatocellular carcinoma with tumor thrombi in right atrium: using cardiopulmonary bypass and deep hypothermic circulatory arrest. J Surg Oncol 2000;74:227–2231. 12. Clayman RV Jr, Gonzalez R, Fraley EE. Renal cancer invading the inferior vena cava: clinical review and anatomical approach. J Urol 1980;123:157–163. 13. Delva E, Barberousse JP, Nordlinger B, et al. Hemodynamic and biochemical monitoring during major liver resection with use of hepatic vascular exclusion. Surgery 1984;95:309–318. 14. Belghiti J, Noun R, Zante E, et al. Portal triad clamping or hepatic vascular exclusion for major liver resection. A controlled study. Ann Surg 1996;224:155–161.