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10.1245/ASO.2004.04.027
Annals of Surgical Oncology 11:714-719 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Prognosis of Lymph Node Metastasis in Soft Tissue Sarcoma

Kasim A. Behranwala, MS, DNB, FRCS (Ed), FRCS (Glas), Roger A’Hern, MSc, Al-Muderis Omar, BSc and J. Meirion Thomas, MS, FRCS, FRCP

From the Sarcoma and Melanoma Unit, Royal Marsden NHS Trust, United Kingdom.

Correspondence: Address correspondence and reprint requests to: Kasim A. Behranwala, MS, DNB, FRCS (Ed), FRCS (Glas), Sarcoma and Melanoma Unit, Royal Marsden NHS Trust, 203 Fulham Road, London SW3 6JJ, UK; Fax: 44-0-20-7808-2673, E-mail: kbehranwala{at}hotmail.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: We defined the tumor characteristics and prognosis of patients with regional lymph node metastasis (RLNM) from soft tissue sarcoma.

Methods: All patients with RLNM from soft tissue sarcoma were identified from the Royal Marsden Hospital Sarcoma Unit prospective database from January 1990.

Results: A total of 73 (3.4%) of 2127 patients had RLNM. Fifty-seven patients (78.1%) had RLNM as the first site of spread, and 16 patients (21.9%) presented with RLNM and distant metastasis synchronously. The most common histologies were rhabdomyosarcoma, epithelioid sarcoma, and angiosarcoma. There were 9 T1 and 36 T2 tumors, and tumor size was not available in 28 patients. There were 6 grade 1, 16 grade 2, and 51 grade 3 tumors. Forty-two patients presented with RLNM along with the primary tumor. Of the remaining patients, the median time to development of RLNM from diagnosis of the primary tumor was 13.5 months (95% confidence interval [CI], 1–100 months). The 1-year survival for patients with isolated RLNM was 77.49% (95% CI, 62.99%–86.88%), compared with 36.27% (95% CI, 13.32%–60.04%) for patients who presented with RLNM and distant metastasis (P = .005). The 1-year survival for metachronous and synchronous RLNM was 94.44% (95% CI, 66.64%–99.20%) and 67.54% (95% CI, 47.89%–81.12%), respectively (P = .05).

Conclusions: Lymph node metastasis is rare. Patients who present with isolated RLNM have an improved survival compared with patients who present with regional and distant metastasis at diagnosis. Synchronous RLNM with the primary tumor have a poorer outcome than metachronous RLNM in the absence of distant metastasis.

Key Words: Lymph node metastasis • Soft tissue sarcoma • Prognosis • Survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Soft tissue sarcomas (STS) mainly spread through the bloodstream to the lung.1,2 The major prognostic factors for STS are size, grade, histological subtype, depth, anatomical location, and resection margins.3,4 Because nodal spread in STS is uncommon, there is limited information in the literature about its clinical implications. Collin et al.,5 in 1987, found that positive regional nodes were an independent predictor of poor outcome in a multivariate analysis of 423 patients. According to some reports, histologically positive nodes occur in 9.1% to 10.8% of patients.6 However, the actual incidence is probably7–11 closer to 5%. Three studies12–14 have evaluated the role of regional lymph node metastasis (RLNM) in STS. The confirmation of metastasis in regional nodes seems to be a clinical expression of the biological aggressiveness of the sarcoma, with 5-year survival rates8,9,14,15 between 10% and 23%. The 10-year survival rate has been reported to be 3%.14 Because of its rarity, there is no indication for elective lymph node dissection as part of the initial treatment of STS.5,6,11 The surgical treatment of RLNM is a palliative procedure, because it invariably indicates distant micrometastatic disease.6,13 Mazeron and Suit10 believed that aggressive treatment could bring about long-term survivors. The American Joint Committee on Cancer (AJCC)/International Union Against Cancer (UICC) classifications state that these patients have a poor prognosis and that the outcome of patients with N1 disease is the same as for those with M1 disease. The aim of this study was to evaluate the prognostic significance of RLNM in STS and to further evaluate the findings of previous studies.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Patients
Patients with RLNM from STS were identified from the prospective Sarcoma Unit database at the Royal Marsden Hospital. Data were collected prospectively for all admissions from January 1990 and included demographics, clinical presentation, investigations, treatment, and outcomes. Tumors at the level of or distal to the knee or elbow were classified as distal tumors.

Diagnosis and Treatment
Lymph nodes were evaluated by fine-needle aspiration cytology, core biopsy, or excisional biopsy to obtain histological diagnoses. Occasionally, nodal metastases were discovered incidentally in the resected specimen when the tumor lay adjacent to a lymph node field. Involvement of lymph nodes by disease (>2 cm) was also judged by evaluation of computed tomography scans.

Patients with isolated lymph node metastases were mainly treated by surgery as the primary modality. A few patients with RLNM with suitable histology (primitive neuroectodermal tumor/Ewing’s sarcoma or embryonal rhabdomyosarcoma), a surgically inaccessible location, or extensive unresectable nodal disease, with or without systemic disease, were treated primarily by chemotherapy or radiotherapy.

Pathology
Tumor-related factors, including histological type, size, and grade, were noted. Tumor size was recorded from the pathologic specimen or imaging analysis. Tumors were classified as T1 (<5 cm) or T2 (>5 cm). Tumor grade was classified as low (grade 1), intermediate (grade 2), or high (grade 3) on the basis of the degree of cellularity, differentiation and vascularity, nuclear pleomorphism, number of mitoses per high-power field, and amount of stromal necrosis.

Follow-Up
Careful surveillance was based on guided history and thorough physical examination. Plain chest radiographs were initially performed every 4 months (for the first 2 years if high grade and otherwise for 1 year) and then yearly. Axial imaging studies for detection of recurrence were not part of the follow-up protocol for the patients in this study and were indicated only if a patient was symptomatic or if clinical examination findings were abnormal. Follow-up data are presented as time in months from the diagnosis of nodal disease.

Statistical Analysis
Generic grouping of site was accepted; extremities and superficial trunk were combined. Visceral sites were analyzed as separate, as were the remainder (head and neck, breast, and retroperitoneum). There were therefore three categories: extremity plus superficial trunk, visceral, and the remainder. According to the AJCC 6th ed./UICC 5th ed. guidelines,16 the patient with dermatofibrosarcoma protuberans (DFSP) was excluded from statistical analysis. Analysis of the effect of site, the extent of treatment (radical vs. limited lymph node dissection), and the timing of RLNM detection on survival (synchronous vs. metachronous to the primary tumor) was undertaken with Cox’s regression. Survival after lymph node metastasis was the primary end point. Survival rates were analyzed, and life-table curves were constructed according to the Kaplan-Meier method. The log-rank test was used to compare differences in survival distributions observed in subsets of patients. No adjustment was made for multiple significance tests, because the interpretation of the P values should be evident.17


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Between January 1990 and June 2001, 73 (3.4%) of 2127 patients were identified with regional lymph node involvement during the course of their disease. The median age of the patients was 41 years (range, 16–86 years). There were 35 male and 38 female patients (M/F = .92). The most common histologies associated with RLNM were rhabdomyosarcoma (22.2%), epithelioid sarcoma (18.5%), and angiosarcoma (10.9%; Table 1). There were 9 T1 and 36 T2 primary tumors, and size were not available in 28 patients (seen at our hospital at various stages of follow-up) because it was not available from the referring hospital. There were 6 grade 1, 16 grade 2, and 51 grade 3 tumors. There was a strong association between nodal spread and high grade (70%). The location of the primary tumor was extremities and parietal wall (n = 51), visceral (n = 11), and other sites (n = 11). The tumors with lymph node metastases were more frequently located in the lower extremity than in the upper extremity (sarcomas are usually located in the lower extremity). The appearance of RLNM was related to the proximal location of the sarcoma.


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  		TABLE 1. Histological types of soft tissue sarcoma with regional lymph node metastasis
 
The distribution of primary lesions associated with RLNM was not dissimilar to the distribution of primary lesions according to site (Table 2). The median follow-up of living patients was 9 months (range, 0–123 months). The clinical presentation of patients is explained in Table 3. Forty-two patients had regional lymphadenopathy at the time of primary treatment (of whom seven patients had synchronous distant metastasis). Thirty-one patients developed RLNM after treatment of the primary tumor (of whom nine had synchronous distant metastasis), and the median time to development of RLNM from diagnosis of the primary tumors was 13.5 months (range, 1–100 months).


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  		TABLE 2. Distribution of soft tissue sarcoma with regional lymph node metastasis according to site
 

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  		TABLE 3. Distribution of patients with regional lymph node metastasis (RLNM) relative to the presentation of the primary tumor
 
Lymph nodes were involved on histological review in 65 patients and were demonstrated as sites of disease on radiological examination in 8 patients. Lymph nodes were palpable in 42 patients. The regional lymph node status was histologically confirmed by fine-needle aspiration cytology or preoperative core biopsy in 17 patients. Nineteen patients had in-continuity resection of the lymph nodes along with the primary tumor. Chemotherapy or radiotherapy treated seven of the eight patients in whom lymph nodes were detected radiologically. The treatment of the lymph nodes was not known or not given in two patients. The extent of lymph node dissection was not known in one patient. Radical lymphadenectomy and a limited lymph node dissection (fewer than 4 nodes excised) were performed in 29 and 19 patients, respectively.

Simultaneous distant metastasis at the time of presentation of RLNM was present in 16 patients. Therefore, the basic series to evaluate the prognostic significance of regional lymph node involvement consisted of 56 patients (excluding 1 patient with DFSP) who had isolated RLNM at the time of their discovery. Of these, 31 went on to have distant metastasis after treatment of lymph node metastasis, with a median time to development of distant metastasis of 21 months (range, 7–35 months). At last follow-up, 10 patients were healthy, 48 patients had died of disease, 12 patients were alive with disease, and 3 patients were dead because of medical reasons.

Survival From Lymph Node Metastasis
No survival difference was observed among the various sites of the primary tumor with RLNM. Thus, the entire group could be studied as a whole irrespective of disease site. The 1- and 2-year survival for patients with isolated RLNM were 77.49% (95% confidence interval [CI], 62.99%–86.88%) and 47.36% (95% CI, 32.67%–60.69%), respectively. The 1- and 2-year survival for patients with distant metastases present at the time of presentation of RLNM were 36.27% (95% CI, 13.32%–60.04%) and 21.76% (95% CI, 5.31%–45.29%), respectively (P = .005; Fig. 1). The 5-year survival for patients with isolated RLNM was 23.9% (95% CI, 12.6%–37.1%) and was 0% for patients who presented with RLNM and distant metastasis.



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  		FIG. 1. Comparison of the N1M1 and N1M0 groups. HR, hazard ratio; CI, confidence interval; Chis, {chi}2; LN, lymph node.

 
Further evaluation was performed only on the 56 patients with isolated RLNM. The age, grade, and size were not significant predictors of survival. Patients treated by surgery had a much better outcome than patients treated by chemotherapy and radiotherapy (P = .005). There was no survival benefit for the patients who had a radical lymphadenectomy compared with the patients who had a limited lymph node dissection (P = .71). The 1-year survival for metachronous and synchronous RLNM was 94.44% (95% CI, 66.64%–99.20%) and 67.54% (95% CI, 47.89%–81.12%), respectively, and the 2-year survival was 55.56% (95% CI, 30.51%–74.75%) and 42.66% (95% CI, 24.67%–59.53%), respectively (P = .05). Metachronous RLNM have a better outcome than synchronous RLNM at the time of diagnosis of primary STS (Fig. 2). The difference in death rates occurs in the first year; the curves then converge in the next 6 months and are similar from 18 months onward.



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  		FIG. 2. Survival curves comparing synchronous versus metachronous lymph node presentation (for isolated regional lymph node metastasis [RLNM] at presentation without distant metastasis). HR, hazard ratio; CI, confidence interval; Chis, {chi}2; LN, lymph node.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
Regional lymph node involvement by STS is uncommon in adults. Although nodal disease is recorded in the staging system, it has a limited effect because of infrequency. The published incidence of lymph node involvement varies widely according to histological type, grade, and disease stage. Our incidence of 3.4% agrees well with the study by Fong et al.12 It may be that for certain tumor characteristics, metastases occur simultaneously via the lymphatic and hematogenous routes.13 Certain histological types have a relatively high incidence of lymph node metastases, i.e., clear cell sarcoma, epithelioid sarcoma, synovial sarcoma, malignant fibrous histiocytoma, angiosarcoma, and rhabdomyosarcoma.6,10,12,14,15,19 The frequency of undifferentiated sarcoma, angiosarcoma, and epithelioid sarcoma was pronounced in the study by Ruka et al.14 In our study, rhabdomyosarcoma, epithelioid sarcoma, and angiosarcoma were common. With the addition of our case, only six documented cases of lymph node metastasis from DFSP have been reported in literature.19,20 The result derived by Ruka et al.14—that the appearance of lymph nodes was not necessarily induced by an increase in the size of the lesion—could not be confirmed, because tumor size was not available in some of our patients.

Fine et al.21 commented that regional lymphadenopathy seldom manifests clinically at the time of initial therapy and that on occasion it becomes evident years after the primary tumor has been excised or has recurred locally. In our study, 42 of 73 patients presented with RLNM synchronously with a primary tumor (7 had synchronous distant metastasis). Certainly, the clinical impression that elective lymphadenectomy is not warranted for STS is supported by the low incidence (3.4%) of nodal metastasis found in this study. Radiotherapy is not given prophylactically to the lymph node–draining areas in sarcoma. Regional lymph nodes as the first site of disease recurrence was observed in 31 (1.5%) of 2127 cases. There was a borderline significance in 5-year survival between local recurrence and regional lymph nodes as the site of first recurrence of disease in the study by Vezeridis et al.15 The presence of RLNM seems to be associated with a high incidence of relapse in metastatic sites and with poor outcome.

The 5-year overall and disease-free survival for stage III in the Memorial Sloan-Kettering Cancer Center study (AJCC 6th ed.) were 56.29% and 51.77%, respectively. The 2- and 5-year survival for patients with isolated RLNM for extremity STS in our study were 47.36% and 23.9%, which was less than with patients with stage III disease. Concomitant distant metastases significantly altered survival for patients with lymph node metastases in our study (2-year survival, 21.76%; 95% CI, 5.31%–45.29%). In the study by Billingsley et al.,22 the 2- and 5-year survival for patients with pulmonary metastases were 30% and 16%, respectively. The 2- and 5-year survival from the Royal Marsden Hospital Sarcoma database for the group with only distant metastases were 36.7% (SE, 2%) and 18.5% (SE, 2%), respectively. These findings suggest that the current AJCC/UICC staging system for STS should be re-examined. Patients with isolated RLNM could be assigned to stage IVa and those with distant metastases to stage IVb.

The conclusion derived by Fong et al.12—that radical lymphadenectomy is appropriate treatment for isolated metastases to the regional lymph nodes and may provide long-term survival—is confounded by the fact that 12 of the 16 patients in the limited lymphadenectomy group had unresectable disease or distant metastatic disease.

In our study it was demonstrated that primary surgical treatment of lymph nodes gives a better survival than that for patients treated by chemotherapy and radiotherapy in the group with RLNM only. Patients treated only by chemotherapy and radiotherapy did worse, probably because they presented with worse disease (higher tumor burden) than those treated with surgery. Limited regional node dissection was performed at referring hospitals or for positive lymph nodes detected incidentally on histology when they were removed in continuity with the primary tumor. Radical lymphadenectomy did not confer a significant survival benefit over limited involved regional node dissection for patients with only RLNM in this study. The possible explanation would be that involvement of lymph nodes, irrespective of the number involved, translates into equal biological aggressiveness. The data are not statistically significant because the numbers are small, and we would still recommend radical lymphadenectomy for treatment of RLNM.

Three patients in our series received adjuvant treatment (two patients were treated by chemotherapy, and one received radiotherapy to the lymph node basin). The combined multimodality therapy did not seem to improve survival rates in our patients, although it is difficult to assess its effect because it was not applied in a randomized fashion. Thus, the data according to adjuvant treatment are not shown and are not discussed further. Forty of 48 patients in our series died of disseminated disease. Therefore, adjuvant chemotherapy after lymphadenectomy may be the most reasonable treatment. Lymph node involvement in sarcoma patients is a poor prognostic sign, and such patients require systemic therapy in an attempt to control future development of metastatic disease.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Lymph node metastasis is rare in STS and is related to ultimate survival. Our results confirm that regional lymph node involvement is an important prognostic factor in STS. Patients who present with isolated RLNM have an improved survival compared with patients who present with regional and distant metastasis at diagnosis. Patients with isolated RLNM at the time of diagnosis of the primary tumor have a poorer outcome than patients who develop isolated RLNM during the course of their disease.


   FOOTNOTES
 
There was an incidence of 3.4% regional lymph node metastasis in soft tissue sarcoma. The 1-year survival for patients with isolated regional lymph node metastasis (RLNM) was 77.49%, compared with 36.27% for patients who presented with RLNM and distant metastasis (P = .005).

Received for publication April 28, 2003. Accepted for publication March 26, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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