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10.1245/ASO.2004.12.039
Annals of Surgical Oncology 11:1079-1084 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

A Critical Assessment of Adjuvant Radiotherapy for Inguinal Lymph Node Metastases from Melanoma

Matthew T. Ballo, MD, Gunar K. Zagars, MD, Jeffrey E. Gershenwald, MD, Jeffrey E. Lee, MD, Paul F. Mansfield, MD, Kevin B. Kim, MD, Luis H. Camacho, MD, Patrick Hwu, MD and Merrick I. Ross, MD

From the Departments of Radiation Oncology (MTB, GKZ), Surgical Oncology (JEG, JEL, PFM, MIR), and Melanoma Medical Oncology (KBK, LHC, PH), The University of Texas M. D. Anderson Cancer Center, Houston, Texas.

Correspondence: Address correspondence and reprint requests to Matthew T. Ballo, MD, Department of Radiation Oncology, Box 97, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030; Fax: 713-563-2331; e-mail: mballo{at}mdanderson.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Although patients with inguinal or pelvic lymph node (LN) metastases from melanoma may develop regional recurrence after dissection, the role of adjuvant radiotherapy remains controversial.

Methods: The medical records of 40 patients with inguinal and/or pelvic lymph node metastases from melanoma were reviewed retrospectively. Indications for adjuvant radiotherapy included the following nodal characteristics: extracapsular extension, LNs ≥3 cm in diameter, ≥4 involved LNs, and LN recurrence after prior nodal surgery. Thirty-seven of 40 patients underwent formal LN dissection. Three patients had only local excision of gross disease for recurrence after prior dissection. All patients received radiation to a median dose of 30 Gy at six Gy/fraction delivered twice weekly.

Results: With a median follow-up time of 22.5 months, the 3-year actuarial distant metastasis–free and overall survival rates were 35% and 38%, respectively. The 3-year regional control rate was 74%. Univariate analyses of patient, tumor, and treatment characteristics failed to reveal any association with distant metastasis–free survival, overall survival, or regional control. Regional failures occurred in nine patients; seven of these were isolated dermal failures within the field of irradiation. Only two patients (5%) had LN basin recurrences; one of these patients also developed dermal recurrence. Fifteen of 40 patients developed lymphedema; in seven of these, lymphedema was present before initiation of radiation therapy.

Conclusions: Radiation may prevent recurrence of nodal disease in patients at high risk for regional failure, but in-field dermal recurrences may sometimes occur (8 of 40, 20%). Treatment-related lymphedema and death from metastatic melanoma were common.

Key Words: Lymph nodes • Melanoma • Radiation


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
At The University of Texas M. D. Anderson Cancer Center (MDACC), primary indications for considering adjuvant radiation therapy after resection of nodal metastases from melanoma have included extracapsular extension (ECE), large lymph node size, multiple involved lymph nodes, and recurrent nodal disease after prior regional nodal surgery.1–9 After surgical dissection alone, regional failure rates ranging from 30% to 50% have been reported when one of these high-risk clinical-pathologic features is present. In contrast, regional recurrence rates after adjuvant radiation therapy for these same clinical situations have been reported to range from 5% to 20%.10–18 Although these data are not from randomized clinical trials, they suggest an improvement in regional control through the selective use of radiotherapy.

Any justification for adjuvant therapy, however, must also balance these apparent improvements in disease control with the risk of long-term toxicity. Unfortunately, direct comparisons between series examining surgery alone and those examining adjuvant irradiation are difficult because the latter tend to include patients with more advanced disease who require more extensive dissection. There may also be differences in the rate of long-term toxicity after combined-modality therapy for different nodal basins. As an example, the risk of clinically significant lymphedema after surgery alone is higher after inguinal or pelvic lymphadenectomy than after axillary or cervical lymphadenectomy.19 Furthermore, it is generally assumed that adjuvant irradiation increases the rate of chronic lymphedema further. If this is true, then the risk/benefit ratio of adjuvant irradiation for patients with inguinal or pelvic lymph node metastases may differ from those with metastases to other lymph node sites, and indications for treatment should differ as well. The purpose of this study was to examine outcome and determine the incidence of complications in patients with inguinal and/or pelvic lymph node metastases from melanoma who have undergone surgical resection and adjuvant radiation therapy.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients were identified through a search of the MDACC Department of Radiation Oncology database. Between 1989 and 2002, 40 patients were identified with inguinal and/or pelvic lymph node metastases from melanoma who were treated with gross total surgical resection and radiation. No patient had visceral metastases at the time of irradiation. Permission to perform this retrospective review and a waiver of informed consent were obtained from the institutional review board.

The duration of follow-up for the 18 patients alive at last contact ranged from 3.6 to 107 months, with a median of 22.5 months. Regional disease relapse was defined as any evidence of tumor regrowth within the ipsilateral inguinal, internal iliac, or external iliac lymph node regions (nodal-type recurrence) or if there was dermal recurrence in or near the field of irradiation. Paraaortic or contralateral inguinal or pelvic lymph node or visceral organ disease recurrences were scored as distant metastatic disease.

Complications were retrospectively classified and data were extracted from the hospital charts. Degree of symptomatology was classified as follows: grade 1, asymptomatic finding noted at the time of follow-up physical examination (e.g., lower-extremity edema documented by the physician in a clinic note, but no therapy necessary); grade 2, symptomatic finding requiring any form of medical therapy (e.g., prescription for pain medications, use of a compressive stocking for lymphedema, or dressing changes for delayed wound healing); and grade 3, requiring surgical intervention.

Actuarial data for regional control, disease-free, distant metastasis–free, overall, and complication-free survival curves were calculated by the Kaplan–Meier method, and tests of significance were based on the log-rank statistic. The significance of differences between proportions was tested with the {chi}2 statistic or with the Fisher exact test, as appropriate.20,21 Factors examined in univariate analysis included age, sex, body mass index, Breslow thickness, Clark level, site of disease (skin, superficial inguinal, or pelvic), extent of nodal disease (number of lymph nodes involved, size of lymph nodes, and ECE), disease presentation (primary or recurrent), and treatment delivered (number of lymph nodes removed, extent of surgical dissection, and extent of radiotherapy fields).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient, Tumor, and Treatment Characteristics
Patients’ ages at the time of surgery ranged from 25 to 79 years (median, 55 years). There were 21 male and 19 female patients. The primary site was unknown in 3 patients, on the trunk in 12, and on a lower extremity in 25. For the 31 patients in whom the Breslow thickness was known, the median was 4 mm (range, 0.5–19 mm). The Clark level was as follows: Clark level II for 2 patients; III for 3 patients; IV for 22 patients; V for 7 patients; and unknown for 6 patients.

Body mass index (BMI) was categorized according to the National Heart, Lung, and Blood Institute definition of normal weight (BMI <25 kg/m2), overweight (≥25 kg/m2 but <30 kg/m2), and obese (≥30 kg/m2). There were 15 patients, 19 patients, and 6 patients in the respective groups. The BMI for all patients ranged from 15.8 to 43 kg/m2 (median, 26.5 kg).

All patients in this study developed metastatic disease within the inguinal and/or pelvic lymph nodes and underwent surgical resection for this disease at MDACC. Nodal disease was documented in the superficial inguinal basin in 26 patients (65%) and in the pelvic lymph nodes (i.e., iliac and/or obturator) in three patients (7.5%). Eleven patients (27.5%) had both superficial inguinal and pelvic lymph node metastases. Only three patients were found to have nodal disease at the time of sentinel lymph node biopsy, but subsequent completion lymph node dissection disclosed extensive nodal involvement. All other patients presented with clinically or radiographically apparent disease.

Thirty-seven patients underwent formal lymph node dissection of the involved nodal basin: superficial inguinal dissection in nine patients and ilioinguinal in 28. For the three remaining patients, recurrence had involved an isolated inguinal lymph node after previous formal dissection, and the surgery at MDACC was local resection of clinically evident disease only.

For all patients, a median of 15 nodes were removed (range, 1–39 nodes) and a median of three nodes were involved (range, 1–21). The median metastatic nodal diameter was 3.7 cm (range, 0.8–26 cm). Table 1 summarizes the characteristics of nodal disease at the time of surgery. All patients had nodal disease with extracapsular extension, a lymph node measuring at least 3 cm in diameter, at least 4 involved lymph nodes, or recurrence after previous dissection for nodal disease.


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  		TABLE 1. Extent of nodal disease prior to radiation
 
Regional irradiation was delivered a median of 2 months following surgical resection of the nodal metastatic disease. For 39 patients the dose was 30 Gy at six Gy per fraction delivered twice weekly (Monday and Thursday and Tuesday to Friday). One patient received 54 Gy at 1.8 Gy per fraction, delivered once a day. Radiation was delivered by either high-energy electron or megavoltage photon beams (≥6 MV), depending upon the depth of the target (e.g., electrons for patients requiring superficial inguinal lymph node treatment only). In general, the policy was to deliver radiation to sites of pathologically confirmed disease. The target was the superficial inguinal lymph nodes only in 30 patients and the superficial inguinal lymph nodes and pelvic lymph nodes in 10. Four patients had minimal pelvic disease and radiation was delivered to the superficial inguinal lymph nodes only.

Adjuvant systemic therapy was delivered to 16 patients (40%). For 7 patients systemic therapy was cytotoxic chemotherapy, while 7 patients received immunotherapy only (interferon, 6; vaccine, 1), and 2 patients received both.

Outcomes
At the median follow-up of 22.5 months, 27 patients had developed subsequent recurrent disease and 22 patients had died; the 3-year actuarial disease-free and overall survival rates were 27% and 38%, respectively. Distant metastatic disease developed in 23 patients, yielding a 3-year distant metastasis–free survival rate of 35%. The median time to development of distant failure in these 23 patients was 4.8 months (range, 1–19.7 months). There were nine patients in whom regional relapse occurred: two patients developed regional nodal-type recurrence and seven patients developed isolated dermal recurrence. The sites of regional disease prior to adjuvant radiotherapy and at recurrence following radiotherapy are shown in Table 2. The median time to development of a regional failure in these nine patients was 6.2 months (range, 2.2–10 months). The actuarial 3-year regional control rate was 74%, but 94% of all patients were free of regional nodal-type recurrence.


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  		TABLE 2. Site of regional disease at presentation to MDACC and relapse
 
Treatment-related complications were documented in 20 patients (Table 3). The most common complication was lower-extremity lymphedema (n = 15; grade 1, 5 patients, and grade 2, 10 patients). In addition, delayed wound healing and/or wound breakdown was observed (n = 6; grade 2, four patients, and grade 3, two patients). One patient had both lymphedema and delayed wound healing. The 3-year actuarial rate for any complication was 52%, and that for lymphedema was 39%. The 3-year actuarial rate of any grade 2 or 3 (clinically significant) complication was 40%, and that of grade 2 lymphedema was 27%. One half of the patients who were subsequently scored as grade 2 lymphedema had evidence of lymphedema before radiation therapy was initiated.


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  		TABLE 3. Incidence and timing of complications (n = 20)
 
Univariate analysis of patient, tumor, and treatment characteristics failed to reveal any associations with disease-free, distant metastasis–free, or overall survival or regional control. Specifically, there was no association between the extent of surgical dissection, extent of radiotherapy fields (groin only vs. groin and pelvis), or extent of pathologically confirmed disease (number of lymph nodes, size, or ECE) and outcome in this cohort.

There was an association between the development of a clinically significant complication (delayed wound healing/breakdown or lymphedema) and BMI. At 3 years, 55% of patients with a BMI of 25 kg/m2 or greater developed a clinically significant complication, compared with 26% of patients with a BMI <25 kg/m2 (P = 0.08). When the BMI was 30 kg/m2 or greater, 83% of patients developed a clinically significant complication, compared with 35% if the BMI was <30 kg/m2 (P = 0.03). Similar differences were seen when clinically significant lymphedema was analyzed with use of these same BMI cut-points, but these differences did not reach statistical significance (with BMI <30 kg/m2, 24% developed clinically significant lymphedema; with BMI ≥30 kg/m2, 55% developed clinically significant lymphedema; P = 0.19).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Current practice guidelines at our institution include consideration of adjuvant irradiation for patients with nodal metastases from melanoma following formal lymph node dissection if clinical-pathologic features predictive of a high risk of subsequent regional failure are present. Primary indications for consideration of adjuvant radiation include nodal ECE, large lymph node size, multiple lymph nodes involved with metastatic disease, and recurrent disease after prior nodal surgery.1–9 Regional recurrence rates after surgical dissection alone when any one of these features is present range from 30% to 50%, although higher rates have been reported (Table 4). Additional high-risk features include therapeutic dissection and cervical lymph node location,1,3–6,9 but our practice guidelines still generally reserve radiation for patients who have one of the primary indications. As for the efficacy of adjuvant irradiation, data remain retrospective, but reported recurrence rates after radiation therapy for these same high-risk clinical situations range from 5% to 20% (Table 5). 10–18


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  		TABLE 4. Regional recurrence rates after lymph node dissectiona according to high-risk clinicopathologic characteristics
 

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  		TABLE 5. Regional recurrence rates after lymph node dissection and radiation
 
The results of the present series are mixed, in that although no patient died as a direct result of uncontrolled regional disease, the overall regional failure rate was 26%. This is higher than what has generally been reported in the other adjuvant radiation series (Table 5). While these results may arguably represent only a small improvement over what might have been obtained had these same 40 patients been observed after surgical dissection, the results appear more favorable when one considers the exact site or type of recurrence. As seen in Table 2, only two of our 40 patients (5%) developed actual in basin nodal-type recurrence, which is significantly lower than one would expect following surgery alone. However, seven patients developed isolated regional dermal recurrence. This pattern of failure has been previously described. In one other adjuvant radiotherapy series of 58 patients, there were a total of nine regional recurrences, eight of which were dermal or subcutaneous, similar to what we have reported in the current series.22 In contrast to this, a recent series including patients treated only with surgery showed regional failures to be more evenly distributed between skin or subcutaneous tissues and lymph node sites.23 These observations suggest that radiation therapy is effective at avoiding what it was intended to avoid, in basin nodal-type failures but not dermal failures. It is not clear if this pattern of dermal recurrence is confined to the inguinal or pelvic basin, but in our previous two series of axillary and cervical lymph node metastases from melanoma there were a total of 17 regional failures, and only one of them was a documented dermal failure.11,12 One simple modification of radiotherapy technique for metastases to the inguinal or pelvic lymph nodes might be the judicious use of bolus over the anterior portion of the radiation field. Bolus increases the dose of radiation delivered to the skin by acting as a tissue-equivalent material within the radiation beam. By increasing the skin dose, the use of bolus could potentially decrease the rate of dermal failures, with little increase in the rate of subcutaneous fibrosis.

If one accepts that the current results are an improvement over surgery alone and that regional control might be improved further through minor modification of radiotherapy technique, then adjuvant radiation therapy should be administered to the inguinal region according to the criteria used for other nodal basins.11,12 Unfortunately, there are several other concerns regarding the widespread and routine application of adjuvant irradiation for the inguinal basin. First, it is important to recognize that many of the clinical-pathologic features that predict for a high rate of regional recurrence also predict for a high rate of distant disease, most notably ECE and an increasing number of involved nodes. Second, the published rate of lymphedema after surgery alone for inguinal or pelvic nodal metastases from melanoma ranges from 7% to 28%, which is significantly higher than after axillary or cervical dissection.6,19,24–29 When only those series that specifically report the rate of clinically significant lower-extremity edema (requiring medical management) are examined, the incidence narrows to 10% to 19%.24,25 This is in contrast to a recent Australian series that reported a 48% incidence of clinically significant lymphedema after groin dissection and adjuvant irradiation.30 It seems apparent, then, from the current series and the Australian series that the rate of clinically significant lymphedema is increased in patients receiving adjuvant irradiation to the groin. Whether this is a direct effect of radiation therapy or a result of aggressive surgical dissection for regionally advanced disease cannot be fully resolved. The finding that one-half of the complications in the current series were present before radiation therapy was initiated, however, suggests that this rate of lymphedema is to some extent a consequence of locally advanced disease and its surgical treatment.

In conclusion, a simple assessment of efficacy does not fully address the pertinent issues surrounding adjuvant radiation therapy for the inguinal lymph node basin. While it appears that unmanageable regional recurrence can be avoided through the judicious use of radiation therapy, the high risk of systemic disease and the risk of chronic lymphedema are reason for caution. To balance these competing risks, we recommend reserving adjuvant groin irradiation for those patients with combinations (two or more) of the primary high-risk clinical-pathologic features. This recommendation is particularly appropriate for obese (BMI ≥ 30 kg/m2) patients, for whom the risk of clinically significant complications appears to be increased further. For patients of normal weight, less strict criteria might be appropriate, depending upon the clinical scenario, but the data suggest that the rate of lymphedema after surgery and radiation is elevated for these patients as well. For patients with axillary or cervical lymph node metastases, we continue to advocate adjuvant irradiation when any one of the adverse features is present.11,12

We recommend 30 Gy at six Gy per fraction delivered twice weekly for patients with nodal metastases from melanoma, although an intergroup Australian and New Zealand study is currently examining the role of 48 Gy at 2.5 Gy per fraction.31 Our recommendation is based primarily upon the current series and our experience with patients who have cervical and axillary lymph node metastases, but there is little reason to suspect that one fractionation schedule would be substantially superior to another.


   ACKNOWLEDGMENTS
 
This study was supported in part by grant CA 06294, awarded by the National Cancer Institute, U.S. Department of Health and Human Services.


   FOOTNOTES
 
Radiotherapy can decrease the rate of inguinal or pelvic nodal recurrence after surgical dissection for nodal metastases from melanoma, but in-field dermal recurrences may still occur. The rate of lymphedema is also more common than reported after adjuvant irradiation for other nodal sites.

Received for publication December 17, 2003. Accepted for publication August 9, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Pelvic Lymph Node Dissection Is Beneficial in Subsets of Patients with Node-positive Melanoma
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