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Annals of Surgical Oncology 9:480-485 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Laparoscopic Resection of Large Adrenal Tumors

Dougald C. MacGillivray, MD, Giles F. Whalen, MD, Carl D. Malchoff, MD, PhD, Daniel S. Oppenheim, MD, PhD and Steven J. Shichman, MD

From the Department of Surgery, Division of Surgical Oncology (DCM), and the Department of Medicine, Division of Endocrinology (DSO), Maine Medical Center, Portland, Maine; and the Department of Surgery (GFW, CDM, SJS), University of Connecticut Health Center, Farmington, Connecticut.

Correspondence: Address correspondence and reprint requests to: Dougald C. MacGillivray, MD, Maine Surgical Care Group, PO Box 10990, 887 Congress Street, Portland, ME 04104; Fax: 207-774-9388; E-mail: mesurg{at}poa.mmc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The maximum size of adrenal tumors that should be removed with a laparoscopic approach is controversial. It has been suggested that laparoscopic adrenalectomy is appropriate only for adrenal tumors <6 cm in size. We report our experience with laparoscopic adrenalectomy in patients with adrenal tumors of >=6 cm compared with patients with smaller tumors.

Methods: We retrospectively reviewed a consecutive series of patients who had a laparoscopic adrenalectomy. Patients were considered candidates for laparoscopic adrenalectomy if their computed tomography (CT) scan showed a well-encapsulated tumor confined to the adrenal gland.

Results: Sixty laparoscopic adrenalectomies were performed in 53 patients. Twelve of the adrenalectomies (20%) were for tumors that were >=6 cm (median, 8 cm; range, 6 to 12 cm). There have been no local or regional recurrences, but one patient with adrenocortical carcinoma developed pulmonary metastases. When the 12 patients with large tumors were compared with the 36 patients with tumors <6 cm, the median operative time (190 vs. 180 minutes; P = .32), operative blood loss (100 vs. 50 mL; P = .53), and postoperative hospital stay (2 vs. 2 days; P = 1.0) were similar.

Conclusions: The size of an adrenal tumor should not be the primary factor in determining whether a laparoscopic adrenalectomy should be performed. Large adrenal tumors that are confined to the adrenal gland on CT can be removed with a laparoscopic approach.

Key Words: Laparoscopic adrenalectomy • Adrenal tumors • Pheochromocytoma • Cushing’s syndrome


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Retrospective studies have shown that patients who underwent laparoscopic adrenalectomy had less postoperative pain, shorter postoperative hospital stays, a faster return to regular activity, and fewer procedure-related complications when compared with patients who had open adrenalectomy.1–5 Many surgeons who have experience with laparoscopic adrenalectomy have adopted this as the preferred approach for the resection of small (<6 cm) adrenal tumors. The laparoscopic approach has not been uniformly accepted as appropriate for the resection of larger adrenal tumors. An adrenal tumor size from 3 to 8 cm (but most often 6 cm) has been given as the upper size limit for laparoscopic adrenalectomy.1,3,6–8 The concerns regarding laparoscopic adrenalectomy for large adrenal tumors are the risk of malignancy and the anticipated technical difficulty with the procedure. In some studies, the size of the adrenal tumor has not been the major factor in selecting patients for laparoscopic adrenalectomy.9–13 We have relied primarily on the computed tomographic (CT) appearance of a well-encapsulated tumor with no evidence of invasion into periadrenal tissues, rather than tumor size, to select patients for laparoscopic adrenalectomy. In this article, we describe our experience with laparoscopic resection of adrenal tumors >=6 cm in size.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This was a consecutive series of lateral transperitoneal adrenalectomies in which the first author was the primary or assistant surgeon. Beginning in September 1993, all patients referred for adrenalectomy were offered a laparoscopic approach if their CT showed the adrenal tumor to be well encapsulated, with no evidence of tumor invasion into surrounding tissues or lymphadenopathy. Neither the size and internal features of the tumor on CT nor the functional status of the tumor was used to exclude patients from having a laparoscopic resection. All patients were evaluated by an endocrinologist and had biochemical testing to determine whether the adrenal tumor was functional.

All laparoscopic adrenalectomies were performed with the lateral transperitoneal approach. The details of this approach have been described.2,14,15 The technique has been modified over the years as experience and equipment have improved. Usually four or five trocars were used for right-sided procedures, and three or four trocars were used for left-sided procedures. Five-millimeter trocars and the 5-mm harmonic scalpel are now used during the dissection and mobilization of the adrenal gland.

After the central adrenal vein was dissected, the 5-mm port that gave the best approach to the vein was exchanged for a 12-mm port to allow for the introduction of a large clip applier or vascular stapler to control the vein before it was divided. Gerota’s fascia was incised, and all fat was cleared from the superior pole of the kidney and from the periadrenal region. Care was taken to identify and preserve any branches of the renal artery in the area of dissection and to leave as large a buffer of periadrenal fat as possible between the adrenal capsule and the laparoscopic instruments. The tissues medial to the adrenal gland were the first to be dissected. This allowed the adrenal gland to remain suspended by the lateral attachments to the abdominal wall and often eliminated the need for retraction of the gland. The capsule of the adrenal gland was never grasped. When the dissection was complete, the adrenal gland was placed into a plastic bag, the incision used for the 12-mm port was enlarged to the appropriate size, and the gland was removed intact. Fragmentation of the gland was never performed.

Operative time was defined as the time from skin preparation to closure of the skin incisions. Operative blood loss was measured from that collected in the suction device. The day of the operation was assigned as day 0 for the determination of postoperative hospital stay. Tumor size was measured on the uncut, fresh specimen with a ruler. Large adrenal tumors were defined as tumors that were >=6 cm in size. Data were accrued from a prospectively maintained laparoscopic adrenalectomy database, office records, and phone contact with the patients or their physicians. The group of patients with large adrenal tumors was compared with the group of patients with tumors <6 cm in size. Comparisons between the two groups were performed with the Mann-Whitney U-test or the {chi}2 test. A P value of <.05 was considered to represent a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Sixty laparoscopic adrenalectomies were performed in 53 patients from September 1993 to November 2000. Unilateral adrenalectomies were performed in 46 patients, and 7 patients underwent bilateral adrenalectomies. Six of the patients who had bilateral adrenalectomies had adrenocorticotropic hormone–dependent Cushing’s syndrome. These patients had adrenal hyperplasia and did not have measurable adrenal tumors, so they were not included in this analysis. The other patient who had bilateral adrenalectomies had an 8.5-cm right adrenal pheochromocytoma and a 3.5-cm cortisol-producing left adrenal adenoma. The characteristics of the 47 patients who had 48 adrenal tumors removed laparoscopically are listed in Table 1. All laparoscopic adrenalectomies were successfully completed. There were no perioperative deaths.


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  		TABLE 1. Characteristics of patients who had laparoscopic adrenalectomy
 
The indication for adrenalectomy and the size of the adrenal tumors for each group of patients are listed in Table 2. The most common indication for laparoscopic adrenalectomy in our series was an aldosteronoma. All of these tumors were <6 cm in size. Patients with pheochromocytoma comprised the greatest proportion (50%) of the group with adrenal tumors >=6 cm in size. These tumors tended to be large, even in the group with smaller tumors, with a median size of 6.5 cm. Ten patients were classified as having nonfunctional adrenal tumors. Two of these patients had slight increases in their preoperative 24-hour urine metanephrines and underwent adrenalectomy for a presumed pheochromocytoma. When pathologic examination of their removed adrenal glands showed no evidence of a pheochromocytoma, they were classified as having nonfunctional tumors. Two other patients classified as having nonfunctional tumors probably had preclinical Cushing’s syndrome. These two patients had no evidence of autonomous cortisol production on their preoperative endocrine evaluation, but they became hypoadrenal after laparoscopic adrenalectomy. Two patients had laparoscopic adrenalectomies performed for known metastatic carcinoma. One patient had an 11-cm adrenal metastasis from a non–small-cell carcinoma of the lung. This patient had severe flank and back pain that progressed despite a course of palliative radiotherapy (38 Gy) to this area. Her pain was completely relieved after laparoscopic adrenalectomy, and she remained pain free until her death from progressive disease. The second patient was receiving treatment for metastatic renal cell cancer. During this treatment, the adrenal metastasis was the only site to demonstrate progression. Laparoscopic adrenalectomy was performed in an attempt to prolong his remission. This patient is alive with stable disease 11.5 months after laparoscopic adrenalectomy. The patients with Cushing’s syndrome tended to have smaller tumors (median size, 3.7 cm). However, the one patient with Cushing’s syndrome and a large (9-cm) tumor had an adrenocortical carcinoma. The CT showed the tumor to be heterogeneous and to have a linear calcification but to be well encapsulated, with no evidence of extension into adjacent tissues and with no evidence of adenopathy. At operation there was no evidence of local invasion or adenopathy. On pathologic examination the tumor weighed 131 g and had areas of necrosis, high-grade cellular atypia, and vascular invasion. There was no evidence of extra-adrenal invasion, and no lymph nodes were found. This patient developed pulmonary metastases 18 months after her adrenalectomy. She is alive with stable pulmonary disease at 42 months after her adrenalectomy. There has been no evidence of local, regional, or trocar site recurrence.


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  		TABLE 2. Indication for laparoscopic adrenalectomy
 
All of the patients who had laparoscopic adrenalectomy had CT that showed their tumor to be well circumscribed, with no findings to suggest infiltration into adjacent tissues and no evidence of regional adenopathy. All of the adrenal glands were removed intact and had negative margins on pathologic examination. However, the patient with metastatic lung cancer did have invasion of the tumor into the extra-adrenal fat. None of the patients have had local, regional, or trocar site recurrence.

Details concerning the operative time, operative blood loss, postoperative hospital stay, and complications are listed in Table 3. There were no differences in these parameters between the groups of patients with smaller and larger adrenal tumors, even though the patients with larger adrenal tumors often seemed to have more difficult and tedious procedures. Our first laparoscopic resection of a 6-cm adrenal tumor did not occur until after we had performed 22 laparoscopic adrenalectomies in patients with smaller adrenal tumors or hyperplastic adrenal glands. Thus, we had considerable experience with this procedure before we encountered patients with larger adrenal tumors, and this may have influenced our results.


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  		TABLE 3. Comparison of outcome measurements
 
The complications that occurred were mostly minor. Two patients with small aldosteronomas had a trocar site infection. Both were treated with oral antibiotics. One of these patients also had a retroperitoneal hematoma. A patient with a 2.5-cm cortisol-producing adenoma had a postoperative supraventricular tachycardia. Three patients had symptomatic hypoadrenalism caused by inadequate corticosteroid replacement. One of these patients had known Cushing’s syndrome caused by a 3.8-cm cortisol-producing adenoma. The other two probably had preclinical Cushing’s syndrome. These patients had adrenal tumors that were 4 and 6 cm in size. The patient who had the seizure was the patient with metastatic lung cancer, who had a known seizure disorder. A patient with a large left adrenal tumor had a serosal injury to the fundus of the stomach during mobilization of the spleen. This was repaired with laparoscopic sutures, and the patient had an uneventful recovery. The patient who had laparoscopic resection of an 8.5-cm right pheochromocytoma and a 3.5-cm left cortisol-producing adenoma had a pneumothorax and pleural effusion after placement of a central venous line. This patient was also the only patient to receive a blood transfusion.

The median follow-up for the entire group of patients was 33 months (range, 4–72 months). The median follow-up for patients with tumors <6 cm in size was 36 months (range, 4–72 months), and for patients with tumors of >=6 cm it was 24.5 months (range, 4–42 months). Three patients, all with tumors <6 cm, were lost to follow-up. There has been complete follow-up for all patients with tumors >=6 cm.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Laparoscopic adrenalectomy has become the preferred method for removing small or hyperplastic adrenal glands. Retrospective comparison studies have consistently shown the laparoscopic approach to have fewer complications, less operative blood loss, less postoperative pain, a shorter postoperative hospital stay, and a faster return to regular activity than open adrenalectomy.1–5 In addition, the laparoscopic approach has been shown to decrease total hospital patient charges for patients having adrenalectomy.16 Despite the success of laparoscopic adrenalectomy in patients with small adrenal tumors, there has been a reluctance to use this approach in patients with large adrenal tumors.1,3,6–8 The maximum tumor size above which a laparoscopic approach is contraindicated has not been determined. However, an adrenal tumor size of 5 to 6 cm or more is frequently given as a contraindication for laparoscopic adrenalectomy.1,3,6,7 The rationale for restricting laparoscopic adrenalectomy to patients with small adrenal tumors has been the potential for malignancy and an anticipated difficult dissection in patients with large tumors. The concern is that that the laparoscopic resection of large adrenal tumors may result in inadequate removal or capsular disruption of a malignant tumor and an increase in the risk of a local or port-site recurrence of the disease.

These concerns are not adequate justification for recommending open adrenalectomy for all patients with adrenal tumors >=6 cm in size. Adrenocortical carcinoma and malignant pheochromocytoma are uncommon, whereas benign adrenal tumors are common. The prevalence of benign adrenal adenomas reported from autopsy series has been from 1.4% to 8.9%.17,18 The estimated annual incidence of adrenocortical carcinoma is two per million people,19 and only approximately 10% of pheochromocytomas are malignant. Although the size of an adrenal tumor has been shown to be an important indicator of the risk of its being malignant, many, if not most, large adrenal tumors are benign.18,20–22 It has been estimated that for patients with adrenal tumors >=6 cm in size, more than 60 adrenalectomies would have to be performed to remove 1 adrenocortical cancer.17 In addition, the risk of malignancy for smaller adrenal tumors may be greater than was previously appreciated. In a recent report, 13.5% of adrenocortical cancers were <5 cm, prompting this group to recommend that laparoscopic adrenalectomy be restricted to patients with functional adrenal tumors <3 cm in size.8 Thus, if size, as the prime predictor of an adrenal tumor’s being malignant, is the sole criterion on which the operative approach is based, many patients with large benign adrenal tumors will have an unnecessary open adrenalectomy, whereas the patients with small malignant tumors will have an inappropriate laparoscopic resection. What is most important is the ability of the surgeon to perform a safe and complete resection of the adrenal tumor, regardless of the operative approach or the size of the tumor.

We have used the CT findings of a well-encapsulated adrenal tumor with no evidence of invasion into surrounding tissue and no regional adenopathy—rather than tumor size, internal imaging features, or functional status—in selecting patients for laparoscopic adrenalectomy. By using these selection criteria, we have been able to perform laparoscopic resection of adrenal tumors up to 12 cm in size. All of these tumors were removed intact and had negative resection margins. Despite the fact that the laparoscopic removal of these large tumors was technically challenging, the optical magnification and directed lighting provided by the laparoscope allowed for the careful and precise dissection of the adrenal glands with a margin of surrounding tissue. This allowed patients who had large adrenal tumors removed to experience the benefits that laparoscopic resection has afforded to patients with small adrenal tumors. There were no differences in the operative time, blood loss, complications, or postoperative hospital stay when this group was compared with the group of patients who had smaller tumors. There were no perioperative deaths, no conversions to open procedures, and no local, regional, or trocar site recurrences in any of the patients. Our results concur with others who have performed laparoscopic adrenalectomy in patients with large or malignant adrenal tumors (Table 4).


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  		TABLE 4. Summary of selected reports of laparoscopic resection of large or malignant adrenal tumors
 
The risk of encountering a malignant adrenal tumor has been the most often cited reason for restricting laparoscopic adrenalectomy to adrenal tumors smaller than 5 to 6 cm in size. The fears that a laparoscopic approach will result in an incomplete tumor resection or increased frequency of local or port-site recurrences are serious but probably unwarranted concerns. Review of the results of laparoscopic resection of large or malignant adrenal tumors in 86 patients from 4 series indicates no reports of local or port-site recurrences Table 4. There are case reports of regional, peritoneal, and distant recurrences after laparoscopic resection of unsuspected adrenocortical cancers.23–28 In these articles, the adrenal tumors were generally within the size range that most would consider appropriate for laparoscopic resection, and all of the tumors were placed into a retrieval bag. Technical factors may have contributed to the recurrence in two of these reports. In one article,24 the tumor was fragmented in the extraction bag, and in the other,25 partial adrenal resection was performed. The recurrence of adrenocortical cancer in the other cases was most likely due to the aggressive biology of the tumors rather than the laparoscopic approach used for their resection.

Wide en-bloc resection of the adrenal tumor and the surrounding periadrenal tissue is important in preventing recurrence and in improving survival in patients with malignant primary adrenal tumors.29 Our experience has shown this to be a consistent accomplishment in the laparoscopic resection of large adrenal tumors (up to 12 cm in size), provided that the preoperative CT shows the adrenal tumor to be well encapsulated, with no invasion into surrounding tissues. Despite the fact that all of our patients had complete resections, one patient had pulmonary metastases after laparoscopic resection of a 9-cm adrenocortical carcinoma. This patient is alive with stable pulmonary disease and no evidence of regional or trocar site recurrence 42 months after laparoscopic adrenalectomy. Adrenocortical cancer is a virulent tumor, and local, regional, and distant recurrence commonly occurs even in patients with small tumors who have had complete resections with open procedures.8,29–31

Laparoscopic adrenalectomy offers advantages, compared with open adrenalectomy, to the patient in terms of less postoperative pain and disability. It also offers advantages to the surgeon in terms of improved lighting, optical magnification, and exposure to an area that is often difficult to access with open operative approaches. The laparoscopic resection of a large adrenal tumor can be technically challenging, particularly when the tumor approaches 10 cm in size. Before attempting laparoscopic adrenalectomy in a patient with a large adrenal mass, the surgeon must have considerable experience with this procedure and a complete understanding of the anatomy of these regions.

The mere finding that an adrenal tumor is >=6 cm in size need not be the primary factor in determining whether a laparoscopic resection is appropriate. If there is no evidence on preoperative imaging studies that the tumor is invasive, then even large adrenal tumors can be safely removed laparoscopically, provided that the surgeon has the requisite skills and experience.

Received for publication March 16, 2001. Accepted for publication March 5, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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