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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2003.04.020 on November 10, 2003

Annals of Surgical Oncology 10:1191-1196 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Metastasis to the Adrenal Gland: The Emerging Role of Laparoscopic Surgery

Abeezar I. Sarela, MB, BS, Ian Murphy, MB, ChB, Daniel G. Coit, MD and Kevin C. P. Conlon, MD

From the Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Daniel G. Coit, MD, Gastric and Mixed Tumor Service, Memorial Hospital, 1275 York Ave., New York, NY 10021; Fax: 212-717-3400; E-mail: coitd{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: It is unclear whether resection of clinically isolated metastasis to the adrenal gland improves survival. Also, the role of laparoscopic adrenalectomy (LA) for metastasis is controversial. This study aimed to (1) identify patients who are most likely to have prolonged survival after resection of adrenal metastasis and (2) compare oncological outcomes of LA and open adrenalectomy (OA).

Methods: A retrospective review of 41 patients, who underwent either OA or LA for metastasis to the adrenal gland during 1997–2002 at a single institution, was conducted.

Results: There were 20 women and 21 men, with a median age of 59 years. The most common disease was non-small-cell lung carcinoma (n = 23), followed by renal cell carcinoma (n = 6). With a median follow-up of 16 months, the overall five-year actuarial survival was 29% (median, 28 months). Four patients were actually alive at four years after adrenalectomy. Disease-free interval (DFI) > 6 months was the only significant predictor of improved survival. LA was performed for 11 patients. There was no difference in the incidence of positive resection-margins or survival between patients with OA or LA.

Conclusions: Adrenalectomy for metastasis, with intent to prolong survival, should be offered to patients with favorable tumor biology, such as those with significant DFI. The oncological outcome from LA appears similar to that from OA.

Key Words: Neoplasm recurrence • Secondary • Laparoscopy • Lung neoplasm • Kidney neoplasm


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It is uncommon to detect metastatic disease that is isolated to the adrenal gland. Such patients present a therapeutic dilemma because there is no definitive evidence that indicates superior outcome with any treatment modality. Few investigators have reported patients who have undergone adrenalectomy for metastatic lesions.1–4 Such series are small, with lengthy accrual periods, and comprise highly selected patients. Notably, a small subgroup of patients achieves prolonged survival after adrenalectomy. Predictors of improved survival in prior studies include prolonged disease-free interval, complete resection, and histological diagnosis of adenocarcinoma.1,3

Laparoscopic adrenalectomy (LA) has several potential advantages in comparison with open adrenalectomy (OA).5 LA may be associated with less intraoperative blood loss, decreased analgesic requirement, shorter length of hospital stay, brief convalescence, and superior cosmesis than OA. LA is currently considered the procedure of choice for benign adrenal disease.5 In contrast, it is contraindicated for primary malignancies of the adrenal gland because of concern for a high incidence of locoregional recurrence.5,6 The role of LA for adrenal gland metastasis remains undefined at present.

A contemporary series of patients who underwent either open or laparoscopic adrenalectomy for metastasis is presented. This study aimed to (1) define the natural history of patients after resection of solitary metastasis to the adrenal gland, (2) identify characteristics of patients who achieved prolonged survival after resection of solitary metastasis to the adrenal gland, and (3) to compare oncological outcomes of LA and OA.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A prospectively maintained, computerized operating-room database was reviewed to identify all patients who underwent adrenalectomy for metastasis during 1997–2002. This period was subsequent to, and mutually exclusive from, the period of a similar, previous series from Memorial Sloan Kettering Cancer Center (MSKCC).3 Clinical, operative, and pathological data were obtained. Data were gathered by retrospective chart review as well as physician, patient, or family interviews.

Disease-free interval (DFI) was defined as the interval between diagnosis of the primary malignant tumor and recognition of adrenal metastasis. Metastases that were recognized within 6 months of primary tumor diagnosis were defined as synchronous (DFI less than or equal to 6 months). Metastases that were recognized at 6 or more months subsequent to primary tumor diagnosis were labeled as metachronous (DFI more than 6 months).

The following exclusion criteria were applied: (1) adrenalectomy performed because of direct extension of a primary tumor to the adrenal gland and (2) adrenalectomy performed simultaneously with ipsilateral nephrectomy for renal cell carcinoma (RCC). Patients with RCC who underwent ipsilateral adrenalectomy for metachronous metastasis and those who underwent contralateral adrenalectomy were included. Metastasis was confirmed to have histopathology similar to the primary tumor.

Open adrenalectomy was performed by either the anterior subcostal approach, thoracoabdominal approach, or posterior approach. All cases of laparoscopic adrenalectomy were performed by a single surgeon, using a transabdominal flank approach. The resection was defined as complete if the specimen-margins were negative for malignancy and the patient had no clinically obvious disease at any other site.

SPSS (version 11) was used for statistical analysis. Summary statistics are presented as median (range) with comparisons using the Mann-Whitney U Test. Overall survival was the interval between the date of adrenalectomy and date of death or last follow-up. Survival analyses were conducted by Kaplan-Meier method with log-rank testing. Cox proportional hazards regression was conducted to identify the prognostic significance of individual variables.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were 41 patients, comprising 21 men and 20 women at median age of 59 years (36–79). Non-small-cell lung cancer (NSCLC) was the most common disease, followed by RCC and then a variety of diseases (Table 1).


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  		TABLE 1. Metastasis to the adrenal gland: disease-type and disease-free interval
 
Some 29% (12 of 41) of patients underwent adrenalectomy for synchronous metastasis, the majority of which were NSCLC (n = 10; Table 1). In 4 of the 10 patients with NSCLC synchronous metastasis, adrenalectomy was performed before resection of the primary tumor. Adrenal metastasis had been detected by fine-needle aspiration cytology in one patient or by positron emission tomography (PET) scanning in the three remaining patients. Two patients subsequently underwent complete resection of the primary tumor. The other two patients with unresected primary tumors were retained in this study because adrenalectomy was performed as part of a potentially curative treatment strategy.

Some 66% (27 of 41) of patients underwent adrenalectomy for metachronous metastasis (Table 1). The median DFI for patients with metachronous metastasis was 30 months (8–199). The DFI for patients with NSCLC (n = 13) was significantly shorter than that for patients with any other disease (n = 14) (13 months [8–37] vs. 61 months [24–199], respectively; P < .001). Nine patients with metachronous adrenal metastasis had previously suffered metastasis to another organ. In all nine patients, nonadrenal metastases had been completely resected at a prior date.

Two patients (5%) had a diagnosis of adenocarcinoma of unknown primary site metastatic to the adrenal gland. Primary adrenocortical carcinoma was definitively excluded by histopathology in both cases. These two patients were not assigned to either the synchronous or the metachronous group.

The left adrenal gland was removed in 19 cases and the right adrenal gland in 23 cases. One patient underwent bilateral adrenalectomies, performed metachronously. There was no postoperative mortality. A complete resection was achieved in 34 patients. The resection margin was microscopically positive for cancer in five cases and the resection was classified as incomplete for these patients. Resection was also classified incomplete for further two patients with NSCLC synchronous metastasis and no resection of the primary tumor. Radiation therapy was administered to one patient with an unresected primary lung tumor and to two patients with positive adrenal-resection margins.

The median follow-up period for the entire group was 16 months (1–62). Sixteen patients were alive and disease-free at a median follow-up of 11 months (1–53) from adrenalectomy. Four patients had undergone complete resection of metastasis at another site, subsequent to the adrenalectomy, and were alive and disease-free at a median follow-up of 26 months (18–62). Three patients were alive with recurrent disease, at a median follow-up of 17 months (9–51), and 18 patients were dead from recurrent disease with a median survival of 14 months (2–35). The overall estimated actuarial survival at 5 years was 29% with a median survival of 28 months (95% confidence interval: 16–40) (Fig. 1).



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  		FIG. 1. Kaplan-Meier plot of overall survival after adrenalectomy for metastasis. Median survival, 28 months; 5-year actuarial survival, 29%.

 
Twelve patients had minimum follow-up for 4 years. Four patients (33%) were actually alive at 4 years after adrenalectomy. Three patients were disease-free at most recent follow-up. One patient had RCC with contralateral adrenal metastasis after a DFI of 49 months and postadrenalectomy survival of 51 months. A second patient with a high-grade spindle cell sarcoma of the jaw had a DFI of 62 months and survival of 53 months. A third patient had NSCLC with DFI of 20 months and survival of 48 months. One patient was alive with recurrent disease (spine metastasis) at 62 months. This patient had RCC with a DFI of 102 months.

On univariate analysis, DFI (< 6 months [synchronous] vs. > 6 months [metachronous]) and disease-type (NSCLC vs. others) were significant predictors of overall survival (Table 2). Age, gender, completeness of resection, and size of the adrenal metastasis did not predict survival. On multivariate analysis, only DFI retained independently significant prognostic value. The overall median survival with metachronous metastasis was significantly longer than that with synchronous metastasis (30 months vs. 12 months, respectively; P = .006) (Fig. 2). All four patients who were actual 4-year survivors had metachronous metastasis.


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  		TABLE 2. Univariate and multivariate analysis of prognostic factors following adrenalectomy for metastasis
 


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  		FIG. 2. Kaplan-Meier plot of overall survival for patients with synchronous metastasis (median survival, 12 months) compared with those with metachronous metastasis (30 months; P = .006).

 
Eleven patients underwent LA. The size of adrenal tumors removed by LA was significantly smaller than those removed by OA (median diameter, 4.5 cm [2.0–12.5] vs. 7.4 cm [2.3–23.0], respectively; P = .008). Synchronous metastasis comprised 36% (4 of 11 cases) of the LA cases as compared with 28% (8 of 30 cases) of the OA cases (P = .7). For metachronous metastasis, the DFI was not significantly different for LA cases than for OA cases (median 41 months [8–199] vs. 17 months [11–63], respectively; P = .3). LA was not converted to open operation in any case. The adrenal tumor was removed intact, without rupture, in all LA cases. There was no postoperative mortality. The length of hospital stay was significantly shorter for patients who underwent LA than for those with OA (median 2 days [1–4] vs. 7 days [2–23]; P = .001). Patients who underwent OA had been under follow-up for a longer period than those with LA (median 42 months [2–69] vs. 21 months [1–43]; P = .01). There was no case of incisional or port-site recurrence. There was no significant difference in overall survival following OA or LA (median survival, 28 months vs. not reached; P = .9) (Fig. 3).



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  		FIG. 3. Kaplan-Meier plot of overall survival for patients who underwent laparoscopic adrenalectomy (median survival not reached) compared with those with open adrenalectomy (28 months; P = .9).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Resection of clinically solitary adrenal metastasis was performed in 41 patients. The 5-year actuarial overall survival was 29% with a median survival of 28 months. In a previous series of 37 patients from MSKCC, Kim et al.3 reported 5-year actuarial survival of 24% and median survival of 21 months. In another series of 52 patients from the Mayo Clinic, Lo et al.1 described 2-year actuarial survival of 40% and, for patients who died, median survival of 13 months.

Whether or not resection of clinically isolated adrenal metastasis alters the natural history of stage IV disease has been previously debated.3 Patients treated by adrenalectomy clearly constitute a highly selected subgroup. The survival characteristics of such patients are compared with those of a reasonably similar group treated by chemotherapy-only in one small series.2 These authors report a median survival of 31 months following adrenalectomy as compared with 8.5 months with chemotherapy-only. Notably, all patients treated without resection were dead by 22 months. Another series reports median survival of only 3 months after radiation therapy for symptomatic adrenal metastasis.7 In the present series, four patients were actually alive at 4 years after adrenalectomy (4-year actual survival: 33%). Kim et al.3 have similarly reported a 5-year actual survival of 21%. Such actual long-term survivors represent a unique biological outcome that is not observed in patients who are treated nonsurgically. In the absence of a randomized clinical trial or large case-controlled series, patients who achieve long-term disease-free survival, a clinical endpoint not seen in nonsurgical series, may be assumed to have derived clinically significant benefit.

One clinically important goal was to determine characteristics that may identify patients most likely to have prolonged survival after adrenalectomy. DFI > 6 months was the only factor associated with improved survival. All patients who actually survived 4 years had DFI > 6 months (i.e., metachronous metastasis). This observation confirms previous work by Kim et al.3 that initially demonstrated the prognostic importance of DFI > 6 months for adrenal metastasectomy. The prognostic value of DFI has been also observed for resection of metastasis from other organs, such as liver metastasis from colorectal carcinoma.8 DFI probably serves as a surrogate marker for the intrinsic biological aggressiveness of malignant disease. Completeness of disease-resection1,3 as well as histological-type (adenocarcinoma vs. all others) have been previously reported as important prognostic indicators.1,3 In the present series, incomplete resection did not emerge as a significant prognostic factor. This may partly be explained by the facts that only seven patients in this series had an incomplete resection and three of these patients received radiation therapy for residual disease. NSCLC was associated with adverse prognosis on univariate analyses but did not retain adverse prognostic value, independent of DFI, on multivariate modeling. This was not surprising, given that almost one-half of NSCLC metastases were synchronous.

Laparoscopic adrenalectomy (LA) was performed for 11 patients. The incidence of microscopically positive resection margins was similarly low for LA and OA. LA was initiated at the authors’ institution about 3 years ago, and follow-up of these patients was shorter than that for OA patients. Nonetheless, during the early follow-up period, survival characteristics for LA or OA patients were similar. Few authors have reported experience with LA for metastasis.6,9–12 Kebebew et al.6 reported 13 patients with adrenal metastasis and five patients with primary adrenal cancer. The median size of the adrenal gland was 4.8 cm (1.5–12), similar to that in the present study. At a median follow-up of 3 years, no patient with metastasis had suffered local recurrence. In contrast, three of five patients with primary adrenal cancer developed local or lymph node recurrence. Heniford et al.9 reported 10 cases of LA for adrenal metastasis. The median size of the adrenal glands was 5.9 cm (1.8–12), and there were no positive resection margins. At mean follow-up of 8 months, there was no local or port-site recurrence. Valeri et al.11 reported six cases of LA for metastasis, with median size of the adrenal glands being 4.5 cm (2.5–6). Once again, there was no local or port site recurrence.

LA has been contraindicated in case of proven or suspected primary adrenal cancer.5 Primary adrenal cancer is a locoregionally aggressive disease, and optimal benefit is achieved by radical excision, including regional lymphadenectomy.13 In contrast, adrenal metastasis are often confined within the adrenal capsule, and simple adrenalectomy may be sufficient to obtain negative resection margins. The present data suggest that well-selected patients with adrenal metastasis can undergo LA without any oncological disadvantage.

Detection of an adrenal mass in a cancer patient often presents a clinical management dilemma. Radiologically guided fine needle aspiration cytology (FNAC) may be performed in order to distinguish malignant from benign lesions. Potential disadvantages of this procedure are a high false-negative rate, bleeding, or a hemodynamic catastrophe if the lesion is a pheochromocytoma.6 Positron emission tomography (PET) scanning has excellent sensitivity and specificity for distinguishing benign from malignant adrenal lesions and appears to the current investigation of choice for cancer patients with adrenal masses.14 LA can serve as an effective staging tool for patients with an inconclusive diagnosis from FNAC or PET scan. Further, in well-selected patients with metachronous metastasis, adrenalectomy may be associated with markedly prolonged survival. Although prolonged survival may be a reflection of tumor biology and careful patient selection, the consistent observation that some patients are cured of their disease is a reflection of the therapeutic impact of the procedure. The present and previous3 data indicate that adrenalectomy for metastasis, with intent to improve survival, is most likely to be successful in patients with a significant DFI. Presently available data on laparoscopic adrenalectomy for metastatic disease are limited, but suggest that there is no oncological disadvantage as compared with open adrenalectomy.


   FOOTNOTES
 
Thirty patients underwent open adrenalectomy and 11 patients had laparoscopic adrenalectomy for metastasis, during 1997–2002. In this highly selected group, prolonged survival was observed only in patients with disease-free interval > 6 months. The oncological outcome with open or laparoscopic resection was similar.

Received for publication April 16, 2003. Accepted for publication August 25, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Lo CY, van Heerden JA, Soreide JA, et al. Adrenalectomy for metastatic disease to the adrenal glands. Br J Surg 1996; 83: 528–31.[Medline]
  2. Luketich JD, Burt ME. Does resection of adrenal metastases from non-small cell lung cancer improve survival? Ann Thorac Surg 1996; 62: 1614–6.[Abstract/Free Full Text]
  3. Kim SH, Brennan MF, Russo P, Burt ME, Coit DG. The role of surgery in the treatment of clinically isolated adrenal metastasis. Cancer 1998; 82: 389–94.[CrossRef][Medline]
  4. Paul CA, Virgo KS, Wade TP, Audisio RA, Johnson FE. Adrenalectomy for isolated adrenal metastases from non-adrenal cancer. Int J Oncol 2000; 17: 181–7.[Medline]
  5. Gill IS. The case for laparoscopic adrenalectomy. J Urol 2001; 166: 429–36.[CrossRef][Medline]
  6. Kebebew E, Siperstein AE, Clark OH, Duh QY. Results of laparoscopic adrenalectomy for suspected and unsuspected malignant adrenal neoplasms. Arch Surg 2002; 137: 948–51.[Abstract/Free Full Text]
  7. Soffen EM, Solin LJ, Rubenstein JH, Hanks GE. Palliative radiotherapy for symptomatic adrenal metastases. Cancer 1990; 65: 1318–20.[CrossRef][Medline]
  8. Fong Y, Cohen AM, Fortner JG, et al. Liver resection for colorectal metastases. J Clin Oncol 1997; 15: 938–46.[Abstract/Free Full Text]
  9. Heniford BT, Arca MJ, Walsh RM, Gill IS. Laparoscopic adrenalectomy for cancer. Seminin Surg Oncol 1999; 16: 293–306.
  10. Smith CD, Weber CJ, Amerson JR. Laparoscopic adrenalectomy: new gold standard. World J Surg 1999; 23: 389–96.[CrossRef][Medline]
  11. Valeri A, Borrelli A, Presenti L, et al. Adrenal masses in neoplastic patients: the role of laparoscopic procedure. Surg Endosc 2001; 15: 90–3.[CrossRef][Medline]
  12. Miccoli P, Raffaelli M, Berti P, Materazzi G, Massi M, Bernini G. Adrenal surgery before and after the introduction of laparoscopic adrenalectomy. Br J Surg 2002; 89: 779–82.[CrossRef][Medline]
  13. Harrison LE, Gaudin PB, Brennan MF. Pathologic features of prognostic significance for adrenocortical carcinoma after curative resection. Arch Surg 1999; 134: 181–5.[Abstract/Free Full Text]
  14. Yun M, Kim W, Alnafisi N, Lacorte L, Jang S, Alavi A. 18F-FDG PET in characterizing adrenal lesions detected on CT or MRI. J Nucl Med 2001; 42: 1795–9.[Abstract/Free Full Text]



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