Thoracoabdominal Adrenalectomy for Malignancy Charles A.G. Proye, MD, FRCS, FRCS Ed. (HON) and Jonathan S. Lokey, MD, FACS
n the 20-year period 1980 through 2000, 47 of 467 (10%) adrenalectomies we performed were via a thoracophrenolaparotomy (TPL) (thoracoabdominal approach), of which 33 were for malignant tumors of the adrenal gland. TPL was the chosen operative approach for 31% of all adrenocortical carcinomas. TPL is well accepted, because it provides excellent exposure, allowing an oncologically correct resection. The approach does, however, have a bad reputation due to common respiratory embarrassment postoperatively. Classically, respiratory capacity is decreased by 30% after thoracotomy, 50% after supraumbilical celiotomy, 40% after infraumbilical celiotomy, and by 70% after TPL. This degree of respiratory embarrassment was observed in the past, when the phrenotomy (division of the diaphragm) was performed radially from the thoracic wall to the diaphragmatic hiatus, thus dividing the fibers of the phrenic nerve. When the diaphragm is divided peripherally, two centimeters from its chest wall insertion, impairment of respiratory function is much less. In addition, TPL is reputed to be one of the more painful operations. This may be avoided by resecting the rib over which the incision is based rather than forcefully retracting the ribs and thereby causing painful fractures. The corresponding intercostal nerve is retracted and not entrapped by the closing suture. In addition to the routine adrenal imaging techniques, in patients with large neoplasms, it is indispensable to have accurate visualization of the venous system to demonstrate, or exclude, involvement of the adrenal and renal veins, particularly on the right side, of the inferior vena cava, because of its retrohepatic portion, and even the right atrium. This is best done by magnetic resonance imaging (MRI) and duplex ultrasonography. TPL is the preferred operative approach for all tumors, right or left, greater than 12 cm in diameter, and for
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From the Professorial Unit of Surgery, General and Endocrine Surgery of the University Of Lille, Lille, France. Address reprint requests to Professor Charles Proye, Clinique Chirurgicale Adults Est, Service de Chirurgie Generale et Endocrinienne, CHRU de Lille, Hopital Huriez, 1 Rue Michel Polonovski, 59037 Lille Cedex, France. Jonathan S. Lokey is currently at Upstate Surgical Specialists, Memorial Medical Office Building Suite 320, 890 West Faris Road, Greenville, SC 29605. Copyright 2002, Elsevier Science (USA). All rights reserved. 1524-153X/02/0404-0112$35.00/0 doi:10.1053/otgn.2002.35351
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right-sided tumors larger than 8 cm in diameter, depending on the patient’s morphology. The more the ribs are aligned vertically and the less they are aligned horizontally, the greater the advantage of TPL over a subcostal laparotomy. However, when tumor thrombus has extended into the suprahepatic vena cava or the right atrium, combined median sternotomy and midline celiotomy (sternolaparotomy), with the possibility of cardiopulmonary bypass, is preferred to TPL. In the absence of venous invasion, the presence of hepatic invasion is a relative indication for a thoracoabdominal versus a subcostal approach. It should be remembered, however, that although both computed tomography (CT) and MRI may underestimate tumor size, it tends to overestimate hepatic invasion. The problems created by arterial and venous vascular anomalies (especially with right-sided tumors), such as the central adrenal vein draining into the suprahepatic vena cava (4% of cases), are no different with the thoracoabdominal approach than with laparotomy.1-3 The major advantage of this approach is to permit complete resection of the adrenal basin; to facilitate lymph node dissections, not only of the interaortocaval region, but especially the retrocaval and retroaortic regions on the right and left, respectively, as well as the ability to resect adjacent organs. This approach also allows precise control of large peritumoral veins, found very posteriorly draining into the perivertebral plexus, easier than with a subcostal laparotomy.4
SURGICAL TECHNIQUE The patient is placed in the lateral decubitus position, with the dependent shoulder being displaced to avoid possible brachial plexus injury. Should the patient be placed in the strict lateral position or should the thorax be reclined posteriorly by 30 to 40°? This depends on the habitus of the patient and the anatomy of the tumor. The more obese the patient, the greater the abdominal volume and the more the patient should remain in the strict lateral position, allowing the abdomen to fall forward, thus limiting compression of the inferior vena cava. Patients with larger tumors and more posteriorly located tumors (especially on the right) should also be positioned in the strict lateral decubitus position to facilitate posterior dissection and rapid control of the vessels (inferior vena cava), as well as division of the greater splanchnic nerve, which allows better forward mobilization of the tumor.
Operative Techniques in General Surgery, Vol 4, No 4 (December), 2002: pp 338-345
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1
Planned incision for left TPL based on the 9th rib.
On the other hand, when hepatic involvement is suspected, the patient is tilted 45° for better control of the hepatic pedicle. When the tumor is not large and the patient not obese, tilting the patient 45° posteriorly is
2
preferred for the comfort of both the surgical and anesthetic teams. To facilitate exposure, the table is flexed in such a manner that the patient’s legs nearly reach the floor while
Right adrenal tumor weighing 2.2kg, exposed by right TPL through the bed of the 9th rib. The lateral aspect of hepatic segment IV is visible to the lower right and the divided diaphragm to the upper left.
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Right TPL. The thoracic cavity can be seen superiorly, the lateral phrenotomy is halfway complete, and the tumor has been reflected anteriorly as the dissection approaches the inferior vena cava.
the upper body is only mildly inclined. The point of flexion should be at the level of the xiphoid process. The patient’s arm on the operative side may rest freely in front of the patient’s neck, or, preferably, can be placed on a padded armrest leaving the jugular vein available for vascular access. The incision may be based on the 8th, 9th, or 10th rib (Fig 1).4 An incision over the 8th or 9th rib is preferred for tumors that are larger, or more posterior or more cranially situated. When venous involvement is suspected, the 8th rib incision should be used to allow better isolation of the intrapericardial inferior vena cava. The rib is resected in its entirety after the periosteum has been carefully elevated using Semb, Overholt, and Delannoy rongeurs. The intercostal nerve is reflected inferiorly. The rib is divided as far posteriorly as possible to the level of its attachment to the spine. Anteriorly, the costal cartilage should not be subjected to electrocautery, as this causes too much necrosis of the poorly vascularized tissue. It should be divided with a scalpel and not reconstructed at the end of the intervention. With the rib resected, application of the Finochetto retractor allows generous surgical exposure with only gentle pressure on the adjacent ribs (Fig 2). Without rib resection, the forceful retraction that is required can fracture the ribs and will result in significant postoperative pain. The diaphragm is divided peripherally, two centimeters from its thoracic insertion, along the length of the incision. Generally, this carries the phrenotomy posteri-
orly up to, but not including, the diaphragmatic crus, which is preserved. The diaphragm is incised between two rows of horizontal mattress sutures, which provide hemostasis and facilitate reapproximation of the diaphragm at the conclusion of the procedure (Fig 3).
Dissection of the Right Adrenal Gland The hepatic pedicle is encircled with vessel loops. The hepatic flexure and right colon are reflected medially (Cattell maneuver), along with the duodenum and the pancreatic head, far enough to expose the left renal vein. The right lobe of the liver is mobilized by dividing the right triangular ligament, exposing the right lateral aspect of the inferior vena cava (Fig 4). On occasion, one or more accessory hepatic veins are present and must be ligated. The tissue overlying the lateral edge of the vena cava is incised, and this dissection is continued until the right adrenal vein is visualized (Fig 5). Attention should be focused on the possibility of a rare venous anomaly; the right adrenal vein draining directly into the right hepatic vein (4% of patients). The posterior, retrotumoral dissection begins by dividing the splanchnic nerve, allowing medial rotation of the tumor and, by applying traction superiorly to free it from the retrocaval region. Synchronously, lateral and retrocaval, as well as aortocaval, lymph node clearance is performed for en bloc resection. The adrenal vein is doubly clipped or ligated.
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Right TPL. The inferior vena cava is fully exposed. Note the confluence of the right hepatic vein and the vena cava (forceps).
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Malignant right pheochromocytoma. The inferior vena cava is well exposed and the central adrenal vein is encircled by a vessel loop. The forceps are on the right renal vein.
342 The plane of dissection then passes between the inferior pole of the tumor and the superior pole of the right kidney, passing through tissue that is often quite dense but practically never involved in the malignant process. This maneuver should not be done at the beginning of the dissection, as this connection allows the kidney to be retracted inferiorly, facilitating surgical exposure. Ultimately, with the tumor being retracted inferiorly, the surgeon completes dissection of the retrohepatic tissue where the most cephalad extension of the very large tumors may ‘creep.’
Management of Tumor Thrombus If tumor thrombus involves only the adrenal vein and minimally projects into the lumen of the inferior vena cava, a Satinsky clamp is placed laterally, and the junction of the adrenal vein and the vena cava is incised. The tumor thrombus is expelled by inducing mild venous hypertension by hyperinflation of the lungs (Valsalva maneuver). The adrenal vein is divided and the vena cava closed (Fig 6). If the tumor thrombus extends into the inferior vena cava but is confined to the infra-hepatic portion (Stage 1), the following steps are taken. (1) Either a vessel loop or clamp is placed around the left renal vein at its termination. (2) A loop or clamp is placed around the supra-renal inferior vena cava (a clamp is preferred to a loop when the lumbar veins are distended). (3) An additional clamp is placed on the infra-hepatic inferior vena cava, which is used to extract the tumor thrombus. If the tumor thrombus is mobile, one can omit the infrahepatic clamp and have the anesthesiologist hyperinflate the lungs. The resultant venous hypertension will flush the tumor thrombus from the inferior vena cava through a venotomy placed again at the junction of the adrenal vein and the vena cava. Only then, at the first flash of blood through the venotomy, is the infrahepatic vena cava clamped to allow for a lateral venorrhaphy. When the tumor thrombus extends into the retrohepatic vena cava but not into the hepatic veins (Stage 2), the superior clamp cannot be placed infrahepatically. In this situation, the pericardium is opened longitudinally taking care to preserve the phrenic nerve. After finger dissection of the intrapericardial segment of the inferior vena cava, a clamp is placed at this level to effect the same maneuvers described above. One could alternately place a temporary caval clip rather than a suprahepatic clamp. A Fogarty catheter can also be used to deliver the neoplastic thrombus.5 Rarely, if the thrombus is adherent to the vein wall and substantial collateral flow has developed, that portion of the inferior vena cava can be resected without subsequent prosthetic reconstruction because of the rich venous arcade surrounding the left kidney. When the tumor thrombus involves the hepatic veins (Stage 3), total hepatic vascular isolation is required. The hepatic pedicle is clamped (Pringle maneuver). The infe-
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rior vena cava is clamped superiorly, en masse, where it crosses the diaphragm. Due to the full mobilization of the right hepatic lobe, a long vertical cavotomy can be performed to allow extraction of the thrombus. The venotomy is closed and the clamps released in the same order as after vascular isolation for hepatic surgery.6 When the tumor thrombus has reached the intrapericardial inferior vena cava or the right atrium (Stage 4), TPL alone is contraindicated because the maneuvers for thrombus extraction are blind and could result in significant hemorrhage. In this situation, the preferred approach is a combined median sternotomy and midline celiotomy, or sternolaparotomy with cardiopulmonary bypass7-10 rather than veno-venous bypass,11,12 despite the risk of hemorrhage induced by systemic heparinization. Cardiopulmonary bypass can also be performed by TPL on the right side, should an intraoperative shift in surgical strategy demand it.
Dissection of the Left Adrenal Gland The spleen should be preserved. To accomplish this, one must avoid any traction on the short gastric vessels. Thus, the first step is to place two or three laparotomy packs under the dome of the diaphragm above the spleen. This gentle downward mobilization of the spleen relaxes the short gastric vessels and prevents undue traction during the procedure. Dissection of the tumor is begun on the anterior surface by examining the base of the superior mesenteric vessels. There are often nodal metastases here, and invasion of the mesenteric vessels per se renders the tumor unresectable. Note the major difference between right- and left-sided explorations: the right adrenal tumor is approached via its posterior aspect while tumors on the left are addressed from the anterior aspect. The splenic flexure of the colon is mobilized, bringing into view the inferior edge of the tail of the pancreas. This edge is mobilized from left to right, reflecting the splenic vein superiorly and the inferior mesenteric vein anteromedially. This will expose the base of the superior mesenteric vessels (the vascular nutcracker) (Fig 7). Once operability has been confirmed, the tumor is mobilized in a manner similar to the right adrenal gland by dissection of its posterior aspect. The inferior pole of the tumor is freed from its attachments to the superior pole of the kidney, and the left renal vein is exposed at its origin. Management of the left renal vein depends on the presence or absence of tumor thrombus therein, as determined by preoperative imaging and gross operative inspection. If there is no thrombus, dissection of the superior aspect of the vein is performed from left to right with ligation or clipping of the vein and dissection continued medially. If there is tumor thrombus involving the left renal vein (Fig 8), this dissection should not be carried out from left to right, but from medial to lateral, controlling the left
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With the tumor thrombus extracted, and the adrenal vein fully amputated, the stump is controlled by a clamp in anticipation of simple lateral venorrhaphy.
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Left TPL after resection of the mass. Note the reflection of the splenic flexure.
344 renal vein at its insertion into the vena cava and proceeding from right to left. The renal vein may be ligated where it joins the cava in anticipation of an en bloc nephroadrenalectomy. Alternately, one may decide to preserve the kidney. In this case, the left adrenal vein is incised at its insertion into the renal vein and the tumor is expelled by temporary venous hypertension (Valsalva maneuver.) The adrenal vein is amputated and the renal vein closed by lateral venorrhaphy. When there is a large volume of tumor thrombus involving the left renal vein, as shown by preoperative MRI, TPL should be avoided, regardless of the tumor size. In this case, the favored approach is through a bilateral subcostal or chevron abdominal incision. With this incision, the Cattell maneuver can be performed as an initial step, and the left renal vein can be controlled where it joins the inferior vena cava to prevent any tumor embolization. If necessary, the infrahepatic vena cava can be controlled by a clip or clamp, as previously described in the treatment of tumor thrombus arising from the right adrenal gland. The surgeon can then return to the left side, and if the tumor is truly enormous, the incision can be extended as a TPL based on the 9th or 10th rib. Given this perspective, the chevron incision should initially be longer on the right side than the left to avoid an acute angle should the wound be extended into the chest. Synchronously, the adrenal basin and retroaortic areas are cleared of lymphatic tissue. A preaortic lymph node resection is performed by ligating the remaining adrenal vessels and dividing the branches of the semilunar ganglion, keeping this fatty tissue with the specimen. It is at this time that the superior adrenal vein is clipped. A cautionary note! When the dissection ‘arrives’ at the crura of the diaphragm, especially the left crus, the thoracic duct and its branches are vulnerable to injury. Dilated lymphatic connections should be individually ligated with locking clips (Fig 9). Blind dissection in this lymphatic tissue potentially infiltrated by the neoplastic process could result in a prolonged chylous fistula. The retroperitoneum is sprayed with a biological sealant, such as fibrin glue, and one or two closed suction drains are placed. For drainage of the hemithorax, a single thoracostomy tube is generally sufficient. This drain is placed anteriorly, as a pneumothorax is a greater concern than is an effusion. The diaphragm is closed with nonabsorbable figure-ofeight sutures along the length of the phrenotomy. The thoracotomy is closed with care taken to avoid the neurovascular bundle of the resected rib as well as its superior partner. No attempt is made to reapproximate the costal cartilages. The abdominal wall is closed in the customary fashion.
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POSTOPERATIVE CARE Routine anticoagulation is particularly necessary in the case of venorrhaphy. The patient is out of bed the day after the intervention. The thoracostomy tube is generally removed after the abdominal drain, and not in the reverse order, to avoid the appearance of a pneumothorax when the abdominal drain is removed. The nasogastric tube is generally left in place for at least 48 hours. In fact, it is not uncommon to see a prolonged gastric ileus (even after the patient has resumed passing flatus) especially after a left-sided intervention. The presence of flatus does not, in this situation, eliminate the possibility of gastric atony. The nasogastric tube is not removed, even if the patient has had flatus, until the tube has drained less than a liter of gastric content over 24 hours. Enteral nutrition can be resumed soon thereafter. After a laborious dissection, especially on the left but also after a more extensive intervention on the right, one
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Venogram demonstrating tumor thrombus emanating from a left adrenocortical carcinoma extending into the inferior vena cava.
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Right TPL after tumor resection demonstrating abundant use of locking absorbable clips to prevent leakage of lymph or chyle.
may encounter a chylous fistula. For this reason, the abdominal drain is not removed until after the patient has had a meal purposefully rich in fat. To avoid this complication, the use of locking clips such as Absolok clips, (Ethicon, Cincinnati, OH, USA) as opposed to ordinary metallic clips is recommended in dissection near the diaphragmatic crura. Such a fistula may be treated medically with etilefrine chlorhydrate, an alpha-agonist that acts on the muscular fibers of the thoracic duct. This medication is given intravenously by automated syringe 10 mg every 12 hours for five days. Usually, at the end of this period, the fistula has resolved. If not, the treatment can be reinstituted for another five days. Only if this second treatment fails should the patient be placed on a medium chain triglyceride diet of three weeks duration. Only that most exceptional case that has not responded to this three-week dietary regime should be considered for reoperation. When a significant venous resection or extensive thrombectomy has been done, it is prudent to ascertain patency by duplex ultrasound before releasing the patient from the hospital to determine the optimal length of anticoagulant therapy.
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2. Johnstone MB: The surgical anatomy of the adrenal glands with particular reference to the suprarenal vein. Surg Clin North Am 44:1315, 1994 3. Monkhouse WS, Khalique A: The adrenal and renal veins of man and their connections with azygos veins. J Anat 146:105-115, 1986 4. Scott HW Jr: Surgery of the adrenal glands. JB Lippincott 306-309, 1990 5. Benoit G, Dartevelle P: Ablation d’un thrombus cave re´ tro-he´ patique sans abord thoracique. Ann Urol 24:384-385, 1990 6. Huguet C, Caporossi M, Gavelli A, et al: Thrombose ne´ oplasique de la veine cave infe´ riure e´ tendue a` l’oreillete droite en rapport avec un cortico-surre´ nalome. Une nouvelle indication de l’exclusion vasculaire du foie. Ann Chir (Paris) 48:364-369, 1994 7. Hedican SP, Marshall FF: Adrencortical carcinoma with intracaval extension. J Urol 158:2056-2061, 1997 8. Novick A, Kaye M, Cosgrove D, et al: Experience with cardiopulmonary bypass and deep hypothermic circulatory arrest in the management of retroperitoneal tumors with large vena cava thrombi. Ann Surg 212:472-477, 1990 9. Proye CAG, Pattou FN: Adrenocortical carcinoma: Nonfunctioning and functioning. In: Clark OH, Duh QY (ed): Textbook of Endocrine Surgery. Philadelphia, PA, WB Saunders, 1997, pp 490-496 10. Ritchey M, Kinard R, Novicki DE: Adrenal tumors: Involvement of the inferior vena cava. J Urol 138:1134-1136, 1987 11. Baumgartner F, Scott R, Zane R, et al: Modified veno-venous bypass technique for resection of renal and adrenal carcinomas with involvement of the inferior vena cava. Eur J Surg 162:59-62, 1996 12. Burt M: Inferior vena caval involvement by renal cell carcinoma. Use of venovenous bypass as an adjunct during resection. Urol Clin North Am 18:437-444, 1991