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CONTENTS Optimal therapy Factors affecting choice Expert commentary Five-year view Key issues References Affiliations
*Author for correspondence Duke University Medical Center, Box 3457, Durham, NC 27710, USA Tel .: +1 919 684 4157 Fax: +1 919 681 7423 david.albala@duke.edu
KEYWORDS: adrenal surgery, adrenocoritcal carcinoma, laparoscopic adrenalectomy
Adrenocortical carcinoma: role of laparoscopic surgery in treatment
George E Haleblian, Cary Wilson, Daniel Haddad and David M Albalat
Adrenocortical carcinoma is a rare disorder with a prevalence of one case per 1.7 million people and a generally poor prognosis. It accounts for 0.02% of all cancer cases and 0.2% of cancer deaths. Within the past three decades, accurate diagnosis, precise radiologic localization, satisfactory preoperative medical management, appropriate anesthesia and refined surgical techniques have come together to render the surgical management of adrenal abnormalities a safe endeavor with predictable outcomes. While there is a general agreement on the suitability of the laparoscopic approach for benign adrenal lesions, controversy remains regarding the use of laparoscopy for suspected adrenal malignancies. This paper provides an overview of adrenal cancer and reviews the literature on laparoscopic adrenalectomy for cancer, including the operative techniques, indications and contraindications.
Expert Rev. Anticancer Ther. 7(9), 1295-1300 (2007)
Adrenocortical carcinoma is a rare disorder with a prevalence of one case in every 1.7 mil- lion people and a generally poor prognosis. It accounts for 0.02% of all cancer cases and 0.2% of cancer deaths [1-5]. Owing to this rar- ity, there has traditionally been a dearth of information regarding the natural history, pro- gression and optimal management of this dis- order. However, in the last two decades the medical establishment has made major strides in the detection and treatment of adrenocortical carcinoma, employing new biochemical tests, new imaging technologies and new surgical treatment approaches.
While adrenocortical carcinoma is quite rare, the presence of adrenocortical masses is common. It is estimated that more than 3% of people aged over 50 years have adrenal nod- ules. Of these nodules, only a small propor- tion are metabolically active and cause endo- crine disorders. Furthermore, fewer than 1% are malignant. With the advent of newer imaging modalities, such as computed tomo- graphy (CT) and MRI, many adrenal masses are detected incidentally (incidentalomas) and their ideal management is a point of debate. CT and MRI have been shown to be the most
accurate modalities when characterizing adre- nal cortical carcinoma (ACA); however, ultra- sound and PET scans can also be used.
The incidence of adrenal masses is bimodal in age distribution and they are typically diag- nosed before the age of 5 years or between the ages of 40 and 50 years. There does not appear to be a change in prevalence based on sex and no correlation between sex and survival has been determined [6].
When an adrenal mass is detected, it should be characterized as functional or non- functional, and as solid or cystic [7]. Nonfunc- tioning adrenal carcinomas are typically larger than functioning ones and characteristically present at a more advanced stage [8]. Adrenal carcinomas tend to be larger than benign tumors and this factor has been used as an important determinant of malignant potential, although the precise cut-off size for predicting malignancy has been controversial [7].
Belldegrun and associates reviewed six series and found 114 cases of adrenal carcinoma, 105 of which were 6 cm or more in diameter [9]. Aso and Homma reported similar findings in their review of 210 patients with incidentally discovered adrenal masses. All 14 malignant
tumors were over 6.5 cm. Therefore, solid adrenal masses measuring over 6 cm are considered malignant unless proven otherwise by surgery [10].
Biochemical screening studies can easily determine the func- tionality of the mass in question. The preoperative distinction between benign and malignant lesions can be difficult, but there are several clues to the malignant potential. Most adrenal cancers are large and hormonally active, producing excessive amounts of cortisol, aldosterone or adrenal androgens, includ- ing dehydroepiandrosterone, which become apparent in blood and urine samples.
However, as CT or MRI scanning may underestimate the size of an adrenal lesion, surgical removal has been recom- mended for masses over 5 cm. Finding a heterogeneous adrenal mass with contrast-enhanced CT or intermediate or increased signal intensity on T2-weighted MRIs indicates probable malignancy of the adrenal mass. If these features are absent, the likelihood of a nonfunctioning adrenal mass under 6 cm being malignant is 1 in 10,000 [11]. In adrenal imaging with 131I 60-iodomethyl-19-norcholesterol (NP)-59, increased tracer uptake by the nonfunctioning mass indicates that the lesion is probably benign. If a secondary tumor is suspected, fine-needle aspiration may be useful.
Nevertheless, none of these tests can be completely relied on to make the distinction with certainty. This fact has prompted some investigators to lower the threshold for operative removal of nonfunctioning adrenal masses. Others have criticized this approach, cautioning against widening the indications for adrenalectomy merely because a less invasive operative approach is available. For incidentally discovered adrenal lesions, the following criteria are considered reasonable indications for recommending excision [12]:
· Secreting lesion
· Diameter of over 4 cm or an increase in size over time
· CT finding of intratumoral necrosis or irregular margins
· High concentration of dehydroepiandrosterone sulfate
Several therapeutic approaches currently exist for treating adrenal carcinoma. Radiation therapy occurs outside of the body using a linear accelerator to focus high-energy beams directly on the cancer. Brachytherapy is an internal radiation therapy, whereby small plastic tubes filled with radioactive pel- lets are placed next to, or directly on, the cancer. Chemo- therapy is a more widely used approach, and more effective if the cancer spreads, compared with either form of the radiation therapies. Systemic chemotherapy uses drugs administered intravenously or orally. There are many side effects associated with chemotherapy, since it can also damage other normal cells. Comparatively, surgery has the best outcomes and remains the standard of treatment for ACA. Therefore, the remainder of this review will focus on the advent and continuing use of laparoscopic surgery for the treatment of adrenal carcinoma. A detailed discussion of laparoscopic adrenalectomy options, as well as a comparison of laparoscopy versus its open counterpart, is presented.
Optimal therapy
Within the span of a decade, laparoscopic urology has pro- gressed from being an investigative and experimental technique to an established, minimally invasive alternative to several open urologic procedures. Although almost all conceivable open uro- logic procedures have been performed laparoscopically, several minimally invasive techniques are as yet unproven to have an advantage over their counterpart in conventional open surgery. However, several studies have shown laparoscopic adrenalec- tomy to have significant advantages when compared with open adrenalectomy, not only in terms of reduced morbidity for frag- ile patients, but also for decreased hospital stay, lower pain lev- els and shorter convalescence [13]. This has been translated into reduced operative time and reduced overall costs compared with open surgery [7,14].
Virtually every conceivable approach to the adrenal gland has been described. These open techniques include anterior transperitoneal, thoracoabdominal and posterior retro- peritoneal approaches. Unfortunately, substantial morbidity is associated with conventional open procedures and present-day approaches for adrenalectomy are far from perfect. Conven- tional operative methods also cause substantial postoperative pain, disfigurement and prolonged convalescence. There is lit- tle disagreement that conventional surgical techniques should be used in patients with large (>6 cm), functioning adrenal neoplasms or those with suspected local extension involving adjacent organs; however, smaller functioning and nonfunc- tioning masses may be treated with laparoscopic methods, a minimally invasive option for removal. In all instances, regard- less of approach, it is crucial that the surgeon abide by the ten- ets of oncologic adrenal surgery by not manipulating the tumor or adrenal tissue and ensuring an en bloc resection to minimize the risk of tumor seeding.
Current indications for laparoscopic adrenalectomy include nonfunctioning adenomas that are increasing in size or sus- pected of causing local symptoms, pheochromocytoma, Cush- ing’s adenoma, aldosteronomas, angiomyelipomas and medul- lary cysts of the adrenal gland. The laparoscopic approach for malignant adrenal neoplasm remains controversial [15]. As experience with the laparoscopic surgery technique grows, it is becoming the surgery of choice for the care of adrenal masses. However, there remain limitations and great care must be taken when deciding between an open, laparoscopic or hand- assisted laparoscopic adrenalectomy. The size of the mass, rel- ative confinement within the organ and surgeon experience are crucial aspects of such a decision [16]. A low threshold should exist for conversion from a laparoscopic to an open approach, if dissection is difficult, to ensure that the tumor is not violated.
Heniford and colleagues reported on 12 laparoscopic adrenalectomies for cancer or metastasis. The mean tumor size was 5.9 cm (range: 1.8-12 cm). One patient was found to have local invasion of the tumor into the inferior vena cava, and this lesion necessitated open surgery for en bloc resection. These authors believe that improved technical skills now allow
a complete laparoscopic dissection that follows the established principles of open cancer surgery. Thus, with routine use of a nonpermeable retrieval bag, laparoscopic adrenal cancer resec- tion is an acceptable option in the hands of experienced lapar- oscopists [17]. More recently, Walz and colleagues reported on their results of 560 consecutive posterior retroperitoneoscopic adrenalectomies. Of the 560 cases, nine had to be converted to open procedures. A total of 485 patients had primary adrenal tumors but only five of these tumors were ACA. In total, 14 patients had adrenalectomy for metastatic disease, of whom four are alive [18]. In another recent series nine patients under- went laparoscopic adrenalectomy for malignancy (three malig- nant pheochromocytomas, four ACA and two adrenal meta- stases). In two cases, conversion was necessary owing to involvement of adjacent organs. Mean follow-up was 23 months, with seven patients alive and one (ACA) with a recurrence [19].
Criteria for adrenalectomy for metastatic disease are that:
· Primary cancer is controlled or controllable
· Other metastatic disease, if present, is resectable
· Patients are fit enough to tolerate general anesthesia
A factor believed to favor laparoscopic adrenalectomy for metastases is that these lesions rarely penetrate the capsule of the adrenal gland. There have been reports of recurrence of adrenal tumors after laparoscopic resection [20]. Therefore, sur- gical enthusiasm must be suitably tempered and proper case selection is of paramount importance in achieving cure rates that are equivalent to those of open surgery.
Transperitoneal approach
For the transperitoneal approach the patient is placed in a lat- eral decubitus position and access to the abdomen is gained with the Veress needle or the Hasson cannula. Following induc- tion of the pneumoperitoneum, three or four 10/11-mm lapar- oscopic trocars are inserted 2 cm below the costal margin in the respective abdominal quadrant. On the left-hand side, dissec- tion is begun with the upper pole of the kidney by freeing the posterior and lateral attachments of the spleen in the direction of the diaphragm. The spleen is retracted medially and superi- orly with a fan or balloon retractor. The adrenal gland will come into view and its superior aspect is dissected before the dissection is carried over medially. The inferior phrenic arterial branches are secured with titanium clips after mobilization of the superior pole.
The adrenal vein is then dissected free and ligated with at least two clips (FIGURE 1). The inferior portion of the gland is dissected last and the gland separated from the surrounding tissue. The gland is then placed in an entrapment sack and extracted from the abdomen. Dissection of the right adrenal gland is similar. The triangular ligament is dissected free, exposing the inferior vena cava. A fan or inflatable balloon retractor is placed to retract the liver. The superior and medial aspect of the adrenal gland is mobilized first, with care taken to secure small vessels with titanium clips. Meticulous dissection
is essential to prevent tearing of small branches from the infe- rior vena cava. The adrenal vein is isolated and at least two clips are placed before transecting it. The inferior pole of the gland is dissected last. Once the entire gland is free (FIGURE 2), it is placed in an entrapment sack and removed.
Retroperitoneal approach
For a retroperitoneal approach, the patient is placed in the lat- eral position with the kidney rest elevated and the table flexed. A 1.5-cm incision is made at the tip of the 12th rib and blunt dissection is used to gain entry into the retroperitoneum through the thoracolumbar fascia [17]. A balloon dissector is placed in the retroperitoneal space behind Gerota’s fascia and inflated with air to 800 cc to create an adequate working space. The balloon is deflated, positioned more cephalad and reinflated to 800 cc, which creates additional space behind the adrenal gland. The laparoscope can be passed through the inflated balloon device to confirm the correct placement and inflation of the balloon. The psoas muscle, intact Gerota’s fascia and diaphragmatic fibers should be readily visible. Two addi- tional trocars are placed, one each in the posterior and anterior axillary line.
Dissection is begun on the left, near the renal hilum, with an incision in Gerota’s fascia to identify and secure the adrenal arteries arising from the aorta. The inferior and lateral aspects of the adrenal gland are then freed from the renal upper pole. The adrenal vein is identified as it drains into the renal vein, then clipped and divided. The posterior, superior and anterior surfaces of the adrenal gland are sequentially mobilized. The adrenal branches of the inferior phrenic vessels and any other remaining vessels are secured with clips and divided. On the right side, the dissection is similar to that described previously. Particular care should be taken to secure the main adrenal vein that is located along the posteromedial aspect of the gland and which runs horizontally for a short distance before draining into the inferior vena cava. Smaller branches from the aorta and inferior phrenic artery may be discovered and require control during mobilization.
Posterior retroperitoneal approach
The posterior retroperitoneal approach was first described by Walz and colleagues in 1996 [21]. In this approach, after induc- tion of anesthesia and placement of appropriate intravenous lines, the patient is positioned prone on the operating table. Following this, a 1.5-cm transverse incision is made below the 12th rib. The retroperitoneal space is reached and blunt dissec- tion carried out digitally to create a small working space. A total of two additional 5 mm trocars are then placed under digital guidance 4-5 cm medial and lateral to the initial incision, with care taken to avoid the expected course of the subcostal nerve. Following this, a blunt trocar with adjustable sleeve and balloon is inserted into the initial incision and pneumoretroperitoneum achieved to a pressure of 12-25 mmHg.
The retoroperitoneal space is then created up to the level of the diaphragm. The adrenal dissection is then carried out from the lateral aspect of the gland cranially to the diaphragmatic branch. Dissection is then carried out medially. The vessels are identified, clipped and transected. The tissue plane between the upper pole of the kidney and the adrenal is now identified and developed. The specimen is then removed in an Endocatch™ (US Surgical Corp.) bag [21,22].
Factors affecting choice
Open or laparoscopic adrenalectomy?
Increasing experience has expanded the indications for laparo- scopic adrenalectomy. While little controversy exists regarding performing laparoscopic adrenalectomy for primary aldoster- onomas, pheochromocytomas and other hormonally active tumors, experts do not agree on the suitability of the mini- mally invasive approach to primary adrenal carcinoma and tumors of over 6 cm. Godellas and Prinz strongly recommend that all tumors suspected of being malignant are not removed laparoscopically [23]. They argue that laparoscopy may be suit- able for ruling out metastases but that the best opportunity for cure lies with an initial en bloc dissection and they believe this goal is best achieved via open surgery. They recommend open surgery for all lesions over 8 cm because of the likelihood of
malignancy. On the other hand, Winfield and colleagues state that adrenal lesions of less than 6 cm in size suspected of har- boring renal metastases or primary adrenal carcinomas can be dealt with by laparoscopy [24]. However, larger primary adrenal carcinomas would have indistinct dissection planes, making a curative en bloc dissection difficult, if not impossible. Similar to other authors, they recommend open surgery for such lesions. Others have also has expressed concerns regarding laparoscopic adrenalectomy for malignant adrenal tumors. As the capsule of the adrenal tumor is very thin and the lesions friable, Winfield believes a tumor could easily rupture during dissection. Fur- thermore, since these lesions should be removed intact within an entrapment sack without morcellation, Winfield contends that only lesions of 5 or 6 cm in diameter are suitable for lapar- oscopic surgery [25]. However, some institutions have expanded the indications for laparoscopic adrenalectomy as experience has been gained [13].
Henry and colleagues reviewed their experience in France with 150 cases of laparoscopic adrenalectomies performed for small and large adrenal tumors. The initial cohort consisted of 102 laparoscopic adrenalectomies for lesions less than 4 cm of which all the tumors were benign. As experience grew, a second cohort was added (n = 48) of tumors larger than 4 cm. In this second cohort, there were 28 nonfunctional tumors and six malignan- cies, of which three were removed laparoscopically while the remaining three required open conversion. Conversion rates were similar in both groups. In four of the six malignant lesions, malignancy was suspected even at the beginning of the laparo- scopic dissection because of the difficulty of dissection, density of adhesions, consistency of the tumors or unusual vessels over the tumor. The authors state that in cases of suspected malig- nancy, laparoscopy should be considered as a treatment option for tumors as large as 12 cm provided that preoperative imaging studies do not suggest invasive carcinoma [26].
If local invasion is observed at the start of the operation, an open procedure should be performed. Gagner and colleagues reviewed their combined experience of 100 cases of laparo- scopic adrenalectomy from Cleveland and Montreal and believe that laparoscopy should be offered for masses as large as 15 cm in diameter. These investigators see few contra- indications to laparoscopic adrenalectomy, namely invasive adrenal carcinoma, uncorrected coagulopathy, previous sur- gery close to the adrenal gland, pheochromocytomas with metastases to lymph nodes and masses larger than 15 cm in diameter [13].
Transperitoneal or retroperitoneal approach?
Both the transperitoneal and retroperitoneal approaches have been used for laparoscopic adrenalectomy. The transperitoneal approach, which offers better orientation and a wider field for dissection, is certainly advisable during the early learning curve, especially for larger tumors and in obese patients. Miyake and colleagues believe the retroperitoneal approach to be superior to the transperitoneal approach because it resulted in reduced blood loss and faster patient convalescence [27].
Another advantage to this technique in their study was a shorter operative duration on the left side. Bonjer and associ- ates found that blood loss, postoperative analgesia use and recuperation were most favorable in patients undergoing ret- roperitoneal surgery [28]. Hand-assisted laparoscopy offers an excellent alternative to open surgery in patients with large tumors and in obese individuals. It can be argued that, if the laparoscopic incision is to be enlarged at the end of the proce- dure to permit intact removal of a large adrenal mass, the advantage of a larger incision could be utilized from the begin- ning of the procedure. The inclusion of the hand in the opera- tive field greatly facilitates dissection, retraction and intact removal of the adrenal gland. Hand-assisted laparoscopy has gained acceptance as a very useful technique for performing a successful adrenalectomy.
Expert commentary
There are few contraindications to laparoscopic adrenal- ectomy. Whereas invasive adrenal carcinoma and previous surgery in the vicinity of the adrenal gland would prompt a surgeon to proceed to an open operation, the presence of widespread metastases would be an absolute contraindica- tion to laparoscopy. The size of the adrenal lesion should also dictate which procedure - laparoscopy or open surgery - is performed for adrenalectomy. There is no doubt that only
experienced surgeons should attempt to remove masses larger than 6 cm laparoscopically. The transperitoneal and retroperi- toneal approaches appear to be equally efficacious and each technique has its advantages and shortcomings. The hand- assisted technique may be used where difficulty with dissec- tion of larger tumors is anticipated or in obese individuals. As the popularity of laparoscopic surgery grows in conjunction with surgeon experience, it holds a promising future for the treatment of adrenal carcinoma.
Five-year view
Laparoscopic adrenalectomies have become increasingly prev- alent for benign lesions of the adrenal gland. The application of this technique for treatment of adrenocortical carcinoma has a role, but care and skill are required to perform the pro- cedure adequately. Studies have suggested that retroperitoneal approaches may offer many advantages to traditional transperitoneal laparoscopic adrenalectomy but, to date, these procedures are performed primarily for nonmalignant pathol- ogies and by only the most skilled laparoscopic surgeons. Adherence to the principles of oncologic surgery is critical for the successful application of laparoscopic techniques to adre- nal malignancies. As experience in laparoscopy becomes more prevalent, the laparoscopic approach to adrenal surgery will become increasingly common.
Key issues
· Adrenal carcinoma is an exceedingly rare disorder with uniformly poor outcomes if not treated adequately.
· Improvements in biochemical screening and radiographic imaging have made detection and characterization of malignant versus benign adrenal lesions much easier.
· Surgical therapy for adrenal carcinoma has traditionally been conducted via open surgical approaches; however, increasingly, laparoscopic approaches are being introduced.
. Multiple laparoscopic approaches to the adrenal gland are available ranging from transperitoneal to lateral retroperitoneal to prone retroperitoneal.
· Wide excision and negative margins are crucial to a successful resection and, currently, only the most skilled of laparoscopic surgeons offer this approach for adrenal carcinoma.
· As experience and skill in laparoscopy increases, this approach may become more common for the treatment of adrenal carcinoma.
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