E- M 6 ®
Excerpta Medica
The American Journal of Surgery 189 (2005) 405-411 Laparoscopy
Laparoscopic adrenalectomy for malignancy
William S. Cobb, M.D., Kent W. Kercher, M.D., F.A.C.S., Ronald F. Sing, D.O., B. Todd Heniford, M.D., F.A.C.S .*
Carolinas Laparoscopic and Advanced Surgery Program, Carolinas Medical Center, 1000 Blythe Blvd., MEB No. 601, Charlotte, NC 28203, USA Manuscript received April 19, 2004; revised manuscript October 5, 2004
Abstract
The superiority of the minimally invasive approach to adrenal resections has been well documented for benign pathology. With technical advances and increased experience, surgeons have successfully performed laparoscopic adrenalectomies for metastatic and primary malignancies of the adrenal gland. The technique of laparoscopic adrenalectomy as it pertains to malignant lesions is presented. A review of the literature demonstrates the safety and efficacy of laparoscopic adrenalectomy for metastatic colorectal, lung, and renal tumors. For primary adrenal malignancies, radical resections can be effectively performed laparoscopically; however, continued long-term follow-up is needed to establish the minimally invasive technique as the preferred approach. @ 2005 Excerpta Medica Inc. All rights reserved.
Keywords: Laparoscopy; Adrenalectomy; Adrenal gland neoplasms; Adrenocortical carcinoma; Pheochromocytoma; Adenocarcinoma
The laparoscopic approach to resection of the adrenal gland was first reported in 1992 [1]. Since its introduction, the technique has become the preferred modality in the surgical treatment of benign adrenal pathology. Many conventional open techniques are available for adrenalectomy; morbidity is as high as 40%, and mortality ranges from 2% to 4% [2,3]. A number of investigators have compared laparo- scopic with open adrenalectomy for benign disease. A ret- rospective study by Prinz [4] in 1995 demonstrated that laparoscopy has a definite advantage in terms of postoper- ative length of hospital stay and parenteral narcotic require- ments for pain control because most patients require few doses of parenteral narcotic analgesics and can be dis- charged 1 or 2 days after surgery. Other studies have re- ported that patients ambulate sooner, tolerate a diet almost immediately, and resume normal daily activities more quickly. In a previous study documenting follow-up of 100 patients, our group noted no recurrence of endocrinopathy and no wound complications [5].
Laparoscopic adrenalectomy affords a significantly de- creased morbidity, shorter length of hospitalization, more rapid convalescence, and improved cosmesis compared with open resection [6-8]. The decrease in perioperative
morbidity has led many physicians to somewhat liberalize their criteria for elective adrenal resection [7]. With im- proved technological advances in the field and the growing technical experience with benign disease, surgeons have successfully expanded the indications for laparoscopic ad- renalectomy to large, nonfunctioning tumors with the po- tential for malignancy and to metastatic lesions [5,9,10]. A complete laparoscopic dissection that incorporates the prin- ciples of the open technique and the use of an impermeable entrapment sac for specimen removal have further made the laparoscopic approach a reliable technique for malignant tumors.
The adrenal glands are common sites of metastasis for several cancers. In the past, the presence of adrenal spread has implied incurable, systemic disease, and these patients were considered terminal [11,12]. Recently, several case reports of unilateral or bilateral adrenal resection for metastatic lung, colon, breast, and renal cancers have refuted this notion [13- 22]. Adrenal metastasectomy has also been reported for mel- anoma with increased long-term survival [23].
The suitability of the minimally invasive approach to primary adrenal carcinomas remains a topic of debate. Pre- vious recommendations were that tumors suspected of ma- lignancy and those >6 cm not be removed laparoscopically [24]. In the previously mentioned situation, the dissection planes are described as more indistinct, making a laparo- scopic, curative en-bloc resection difficult. However, as
* Corresponding author. Tel .: +1-704-355-3176; fax: +1-704-355- 5619.
experience was gained with this technique, the ability to perform a radical adrenalectomy or nephroadrenalectomy, if needed, has become well described [25].
We describe the technique for laparoscopic adrenalec- tomy, using both the transabdominal and retroperitoneal approach, for metastatic and primary malignancy of the adrenal gland. The radiographic modalities to help distin- guish benign and malignant adrenal pathology are exam- ined. A review of the literature provides analysis of the efficacy of laparoscopic adrenalectomy for primary carci- noma and metastatic disease.
Technique
Transperitoneal approach
A urinary catheter, orogastric tube, and sequential com- pression stockings are used routinely. The patient is placed in the lateral decubitus position with the operative side positioned superiorly. The surgeon and assistant stand fac- ing the anterior surface of the abdomen. Appropriate pad- ding to protect pressure points is used. A soft roll is placed in the axilla and under the flank at the level of the umbilicus. The kidney bridge is elevated and the table flexed to the point that the flank musculature is taut.
Entry into the abdominal cavity is gained at a site 2 cm below and parallel to the costal margin and just medial to the anterior axillary line. A muscle-splitting technique is used, and a 10-mm trocar is inserted. A 30°, 5-mm laparo- scope is used throughout the operation. After adequate pneumoperitoneum (15 mm Hg), 2 additional 5-mm trocars
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are inserted for a left adrenalectomy and 3 trocars for a right-side procedure. The trocars should be placed a mini- mum of 6 cm apart to decrease interference between instru- ments.
A diagnostic laparoscopy is performed first. If visual inspection shows no metastatic disease, a laparoscopic ul- trasound examination is performed (see Imaging Modalities section). At the beginning of the dissection, the scope is positioned in the lateral trocar site, and the working instru- ments are placed in the medial 2 ports.
On the left, the lienocolic ligament is divided as needed to allow medial and inferior retraction of the splenic flexure of the colon. Laterally, the peritoneum is incised 1 cm from the spleen to leave a small peritoneal cuff as a “handle” for retraction. The spleen is fully mobilized cephalad so that it falls medially and does not need retraction. The dissection is carried posteriorly to the tail of the pancreas, which is rotated medially as well. The lateral and anterior portions of the adrenal gland often are visible in the perinephric fat (Fig. 1). The table is further tilted in reverse-Trendelenburg position to allow caudal displacement of surrounding or- gans. The dissection of the gland starts inferiomedially, controlling the left adrenal vein initially, if possible. If the adrenal mass is large (5 to 10 cm), dissecting the lateral and inferior poles before dividing the adrenal vein will allow better mobilization and easier control of the vessel. The main left adrenal vein measures approximately 5 to 10 mm in diameter and is most often controlled with medium-large titanium clips (Fig. 2). The adrenal vein should be traced to ensure that it is not an accessory renal vein. It can also be traced to the left renal vein. An endoscopic gastrointestinal (GI) stapler with a vascular cartridge can be used if the vein
is very large. The adrenal branches of the inferior phrenic vessels are often large and should be ligated. Once the adrenal gland is free, it is placed in an appropriately sized impermeable entrapment sac. The bag is removed by way of the original 10-mm trocar site, which often needs to be enlarged. We do not morcellate adrenal masses to permit evaluation of surgical margins, although it has been de- scribed [7]. Clips can be placed at the operative site if adjuvant radiation therapy is scheduled.
Dissection of the right adrenal gland is performed in a similar manner. A fourth trocar is necessary on the right to retract the liver and expose the most medial aspect of the adrenal gland and inferior vena cava (Fig. 3). The right hepatic lobe must be fully mobilized to expose the junction of the adrenal gland and inferior vena cava. The right lateral hepatic attachments to the retroperitoneum and the triangu- lar ligament are transected using the laparoscopic scissors or an ultrasonic shear. The peritoneum overlying the gland is opened, and the right adrenal vein is dissected first. Early access to the right adrenal vein is available even for tumors >5 cm. With control of the vein, the rest of the adrenal gland is easily mobilized. The dissection begins medially and inferiorly along the lateral border of the vena cava and is continued superiorly. The right renal vein is the inferior extent of the dissection. The right adrenal vein is encoun- tered during the dissection along the vena cava (Fig. 4). This vein is often short, broad, and transversely oriented. The vein can typically be controlled with medium-large tita- nium clips with at least 2 on the vena cava side. If there is not enough length for clips, a 35-mm vascular stapler can be used instead. Often, a smaller, secondary branch is present
VC Sulivan
above the main branch and communicates with the cava. Control of this vessel is obtained in a similar fashion as described. As the dissection continues over the superior portion of the gland, small branches from the inferior phrenic vessels are encountered and can be cauterized with the monopolar hook or clipped as needed. The lateral at- tachments to the adrenal gland are taken down with either the monopolar hook or the ultrasonic coagulating shears (Ethicon, Cincinnati, Ohio). The traditional teaching is that the anterior and posterior surfaces of the adrenal are “avas- cular”; however, in our experience, the magnified view of the laparoscope illustrates small vessels as well as the blood from them if they are divided. Once the adrenal is com- pletely freed, the specimen is removed in an entrapment sac through the 10-mm port site, which is dilated as needed [26].
Retroperitoneal approach
The patient is placed in the full-flank position with the kidney bridge elevated. The table is flexed enough to make the flank musculature feel slightly taut. Initial access to the abdominal cavity is obtained through a 1.5-cm transverse skin incision just below the tip of the 12th rib. The flank muscles are successively split with the S-retractor, and the anterior layer of the thoracolumbar fascia is entered. A balloon dilator is inserted into the retroperitoneal space in the vicinity of the lower renal pole. The balloon is distended to approximately 800 cc. The balloon is deflated and ad- vanced slightly higher in the retroperitoneum toward the upper pole of the kidney, and again the balloon is inflated to 800 cc to allow for adequate working space posterior to the
adrenal gland along the diaphragm. The balloon dilator is removed and replaced with a 12-mm balloon-tipped trocar. Carbon dioxide pneumoretroperitoneum is established at 12 mm Hg, and a 30° or 45° 5-mm laparoscope is introduced. Ready visualization of the psoas muscle and the anteriorly displaced Gerota’s fascia and kidney confirms proper bal- loon placement in the retroperitoneum. Two additional 5-mm ports are placed using laparoscopic or bimanual guid- ance. The locations of the ports are in the posterior axillary line and at the lateral border of the psoas muscle. A fourth port can be placed at the level of the primary port in the anterior axillary line.
Finding the adrenal gland can be difficult in an obese patient undergoing a left adrenalectomy. The use of lapa- roscopic ultrasound aids in localization of the gland. A reliable laparoscopic ultrasound unit should therefore be available whenever performing a left adrenal resection, even for benign disease [27]. Beginning in the region of the renal hilum, Gerota’s fascia is incised transversely toward the upper pole of the kidney using a hook cautery instrument. The adrenal arterial branches arising from the aorta are frequently divided first as the upper pole is dissected. As the dissection continues along the lateral border of the kidney, within Gerota’s fascia, the avascular plane between the upper renal pole and the adrenal gland is easily developed. Complete mobilization of the upper renal pole greatly fa- cilitates retroperitoneoscopic dissection of the adrenal gland. This maneuver allows the kidney to drop posteriorly on the psoas muscle. Next, and if possible, the main adrenal vein is identified at its origin from the left renal vein. Dissection proceeds along the medial aspect of the upper pole of the kidney toward the renal hilum. If identified at this stage, the adrenal vein is clipped and divided. Sequen- tially, the posterior, superior, and anterior surfaces of the adrenal gland are mobilized from the psoas muscle, dia- phragm, and peritoneum, respectively. This step usually involves controlling the adrenal branches of the inferior phrenic vessels along the superior edge and any remaining aortic branches along the anteromedial edge of the adrenal gland. If the main left adrenal vein was not identified earlier, retraction of the mobilized adrenal gland in an anterolateral direction at this point places the attachments surrounding the vein on gentle stretch. Careful dissection with a hook dissector or right- angle instrument clearly identifies the main adrenal vein, which is clip-ligated with 3 clips toward the renal vein. The excised adrenal gland, enclosed in peria- drenal fat, is now placed in the impermeable entrapment sac for removal by way of the primary port site.
On the right side, the only differences are the ease in which the gland is located, even in an obese individual, and the steps to control the main adrenal vein. Finding the gland on the right is much easier than on the left. The vena cava is frequently identified right away and leads the surgeon directly to the adrenal gland. The right adrenal vein is short, horizontal, located along the posteromedial edge of the adrenal gland, and drains directly into the inferior vena
cava. Because of its comparatively posterior location, the right adrenal vein is often visualized earlier during retroperi- toneoscopic dissection between the vena cava and the adrenal gland. Occasionally, there are 2 to 3 smaller veins, in contrast to 1 main adrenal vein, and care should be taken to look for these. Small arterial branches from the aorta and renal hilum are clip-occluded or cauterized when encountered [26].
Hand-assisted approach
Hand-assisted laparoscopy provides a nice alternative to the open technique for large adrenal tumors and obese patients. If the laparoscopic incision must be enlarged to allow for specimen removal, the advantage of a larger in- cision could be used from the outset of the procedure. The efficiency of the hand-assisted approach has been demon- strated by our group for radical and donor nephrectomies. In a series of 119 consecutive patients undergoing laparo- scopic nephrectomy, the hand-assisted approach decreased operative time and blood loss without increasing total hos- pital charges or length of stay compared with pure laparo- scopic nephrectomy. Hand-assisted laparoscopic nephrec- tomy was also associated with fewer postoperative complications than standard laparoscopic nephrectomy (28.2% vs. 6.3%) [28]. The use of the hand during advanced laparoscopic procedures provides the tactile benefits of open surgery with the postoperative advantages of laparoscopy. For adrenalectomy, the hand-assisted technique can facili- tate dissection, retraction, and removal of an intact gland.
Imaging Modalities
In considering laparoscopic adrenalectomy for malig- nancy, preoperative diagnosis is of paramount importance. Conventional modalities such as computed axial tomogra- phy (CAT) or magnetic resonance imaging (MRI) are help- ful in distinguishing benign from malignant adrenal lesions. CAT is the technique of choice for imaging the adult adre- nal glands and has a reported sensitivity of 84%, a speci- ficity of 98%, and an accuracy of 90% in suspected adrenal disease [29]. On CAT, adenomas appear as homogenous lesions with distinct margins. In contrast, malignant lesions are more heterogenous with irregular margins on CAT. In contrast to carcinomas, which have much higher attenuation values, adenomas usually have low attenuation values (<10 HU) [30]. A retrospective analysis regarding the utility of MRI for the preoperative diagnosis of adrenal tumors re- ported sensitivity for the differentiation of benign from malignant adrenal masses as 89%, whereas specificity was 99%, and accuracy was 93.9%. Most adrenal adenomas have a lipid-rich composition in contrast to the lipid deple- tion seen with nonadenomatous lesions [31].
The investigators of this study [27] also employed intraop- erative laparoscopic ultrasound (LUS) to eliminate concurrent intra-abdominal pathology. Laparoscopic ultrasound can be
done immediately after entering the abdomen or after mobili- zation of the spleen or liver. The frequency of the transducer is initially set at 7.5 MHz to allow a maximum of 6 to 9 cm of tissue penetration with resolution to <2 mm. After identifying the gland itself, detailed information concerning the adrenal tumor-including size, internal acoustic appearance, presence of an intact capsule, and the gland’s relationship to the kidney, pancreas, renal pedicle, inferior vena cava, aorta, and other major vascular structures-is gained. The draining vessels of the adrenal are then identified. Color Doppler ultrasound can be helpful in identifying the small vessels surrounding the adrenal gland. Attention is then turned to examine all anatomic sites of the liver, the para-aortic lymph nodes, and the contralateral adrenal gland [27].
Laparoscopic Adrenal Metastasectomy
Once a neoplasm has metastasized, systemic and local- ized treatments, in particular radical surgery, rarely render the patient disease free. However, resection of isolated colo- rectal metastases to the liver and lung has now become standard therapy in selected cases [32,33]. Similarly, sev- eral anecdotal reports have documented prolonged and even 5-year patient survivals after adrenal metastasectomy for renal cell carcinoma, non-small cell lung cancer, and colon cancer [17,34,35]. In a review of the literature, 21 investi- gators reported 38 cases of synchronous or metachronous contralateral adrenal metastases from renal cell carcinoma [26]. In 35 cases, the patients underwent curative adrenal resection. With an average of 26 months of follow-up, 62% of patients have no evidence of renal carcinoma. In a ret- rospective review, Luketich and Burt [11] noted long-term, disease-free survival after resection of isolated adrenal me- tastases from non-small cell lung cancer. Their series of 14 patients suggests that chemotherapy followed by surgical resection might be superior to chemotherapy alone in se- lected patients. All patients who received medical manage- ment alone were dead by 21 months. In the surgically resected group, the 3-year actuarial survival rate was 38% [11]. Based on the experience of Luketich et al [11] and in a review of reported cases, 5-year survival rates of 25% to 40% have been seen in selected patients. As a result of their research, selection criteria for laparoscopic metastasectomy include (1) complete control of the primary lung cancer, (2) an extensive metastatic survey revealing only a solitary metastasis, and (3) the ability of the patient to tolerate general anesthesia.
Several factors support the minimally invasive resection of adrenal metastases. One is the dramatic increase in lapa- roscopic surgery experience. Minimally invasive techniques offer excellent visualization, early control of the organ’s vasculature, and the ability to effectively screen for condi- tions that preclude resection (ie, disseminated disease). These features, combined with the general improvement in outcomes when other cancers have been resected laparo-
scopically, make the transition from open to laparoscopic adrenalectomy a viable consideration [10,15]. Several con- cerns have been raised concerning the often-brittle nature of a cancerous lesion. The possibility of a thin adrenal tumor capsule with tumor rupture caused by aggressive manipu- lation during laparoscopic surgery can fuel fear of dissem- inating malignant cells inside the abdominal cavity. Despite this concern, there have been few reports of wound or adrenal bed recurrences in metastatic lesions.
Another factor that supports the use of laparoscopy is the belief that, most often, simple adrenalectomy is enough to remove metastatic lesions. Ayabe et al [17] observed that metastatic adrenal lesions seldom penetrate through the cap- sule of the gland. When extraglandular extension is found, conversion to laparotomy with extended resection including the involved organ should be performed. In our experience, 13 of 14 metastases resected were contained within the gland. In 1 patient, the tumor penetrated the capsule of the adrenal gland. This operation was converted to open, and an in-continuity resection of the lateral wall of the inferior vena cava was performed to achieve negative margins [26]. Ad- ditionally, a true radical adrenalectomy can be performed laparoscopically if needed.
Few series exist that report experience with laparoscopic adrenalectomy for metastasis. Heniford et al [10] were one of the first groups to document success with this approach. Fourteen laparoscopic resections were performed for adre- nal metastasis in 13 patients; there was 1 case of bilateral metastases. The primary cancers for the metastatic lesions included renal cell (n = 5), lung (n = 5), colon (n = 2), and melanoma (n = 1). The mean size of the tumors was 5.9 cm, and the resection margins were negative in all patients. At a mean follow-up of 12 months, no local or trocar site recur- rences developed. There were 2 deaths from distant metas- tases [26]. Kebebew et al [36] reported 13 patients with laparoscopic resection of adrenal metastases. The mean adrenal metastasis tumor size was 4.8 cm. In all patients undergoing laparoscopic metastasectomy, the tumor resec- tion margins were clear, and there was no invasion outside of the adrenal gland. Four of the 13 patients developed distant recurrences at a mean follow-up of 3.3 years [36]. Sarela et al [20] reported their experience with 11 patients undergoing laparoscopic adrenalectomies for metastatic dis- ease. There was no difference in the incidence of positive- resection margins or survival compared with a similar group undergoing open resection of adrenal metastases [20]. Valeri et al [21] reported 6 cases of laparoscopic adrenal- ectomy for metastasis with median size of the adrenal glands being 4.5 cm. Once again, there was no local or port-site recurrence.
Our experience suggests that there are a few absolute contraindications for laparoscopic adrenalectomy. We con- sider locally invasive disease as a possible contraindication for the laparoscopic approach; it would depend on the extent and complexity of the operation required and the surgeon’s experience. Other contraindications include identification of
other widespread systemic disease and perhaps previous trauma or surgery in the area such as a nephrectomy or splenectomy. These can create dense adhesions that add to the difficulty of the dissection; however, we often have completed these operations successfully. We have not con- sidered previous laparotomy as a reason to forego the lapa- roscopic approach because 69% of our patients had previous surgery, and none were converted due to adhesions. A mass ≥10 cm might also be an additional contraindication, but we have laparoscopically resected adrenal masses as large as 13.8 cm [10].
Laparoscopic Adrenalectomy for Primary Disease
Primary malignant adrenal tumors include adrenocortical carcinoma and malignant pheochromocytoma. The preop- erative diagnosis of such tumors is often difficult. Lesions with a diameter >6 cm are considered a possible malig- nancy. Aso and Homma [37] examined 210 Japanese pa- tients with adrenal incidentalomas and discovered that of the 14 patients with malignant tumors in the group, all had tumors with a diameter ≥6.5 cm. In another series of 114 patients with malignant adrenal lesions, the tumor diameter measured ≥6 cm in 105 patients (92%) [38].
Laparoscopic resection has recently been performed for primary adrenal cancer. A review of the literature revealed 25 cases of primary adrenal carcinoma between 1998 and 2004 reported by 11 investigators [36,39-43]. Local recur- rence or intraperitoneal dissemination occurred in 10 of 25 (40%) patients. The length of disease-free interval was pro- vided for 10 of the surviving patients and averaged 34.1 months.
Obviously, careful consideration should be given to ad- renal tumors that appear to be malignant. If the surgeon is comfortable performing wide resection laparoscopically, it may be suitable to approach these with minimally invasive techniques. It is important to inform the patient of the chances of conversion to open surgery and the possibility of local recurrence after surgery regardless of the technique used (laparoscopic or open).
Comments
Long-term, disease-free survival after adrenal metasta- sectomy for renal, colorectal, lung, and melanoma primary tumors shows promise in some selected patients. By de- creasing the trauma of access, minimally invasive adrenal- ectomy has clear advantages in favor of an open approach. Laparoscopic adrenalectomy for metastases in our cohort appears feasible and safe. The obvious improvement in patient satisfaction and preliminary outcome should not overshadow the primary goals of patient safety and the performance of accepted and established oncologic resec- tion. Only by careful staging and appropriate patient selec-
tion can we assess the efficacy of the laparoscopic method. Although this review shows promise, long-term follow-up is imperative to effectively evaluate minimally invasive techniques as the treatment of choice for metastatic or primary adrenal carcinoma.
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