Annals of Surgical Oncology Cite Track
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
10.1245/s10434-006-9014-z
Annals of Surgical Oncology 13:1216-1223 (2006)
© 2006 Society of Surgical Oncology
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by McHugh, J. B.
Right arrow Articles by Sabel, M. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by McHugh, J. B.
Right arrow Articles by Sabel, M. S.

Original Article

Significance of Multiple Lymphatic Basin Drainage in Truncal Melanoma Patients Undergoing Sentinel Lymph Node Biopsy

Jonathan B. McHugh, MD1, Lyndon Su, MD1,2, Kent A. Griffith, MPH, MS3, Jennifer L. Schwartz, MD2, Sandra L. Wong, MD4, Vincent Cimmino, MD4, Alfred E. Chang, MD4, Timothy M. Johnson, MD2,4,5 and Michael S. Sabel, MD4

1 Department of Pathology, University of Michigan, Ann Arbor, Michigan 48109
2 Department of Dermatology, University of Michigan, Ann Arbor, Michigan 48109
3 Biostatistics Core of the University of Michigan Comprehensive Cancer Center, Ann Arbor, Michigan 48109
4 Department of Surgery, University of Michigan, 3304 Cancer Center, 1500 East Medical Center Drive, Ann Arbor, Michigan 48109
5 Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan 48109

Correspondence: Address correspondence and reprint requests to: Michael S. Sabel, MD, FACS; E-mail: msabel{at}umich.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Truncal melanoma involving metastases to multiple lymph node basins has a much worse prognosis than tumor involvement of a single lymph node basin. Recent results also suggest that, independently of the status of lymph node involvement, patients with multiple lymphatic basin drainage (MLBD) on lymphoscintigraphy have an increased risk of lymph node metastasis and a worse prognosis than those with a single lymphatic drainage basin. Because published reports have conflicting results, the authors compared their experience at the University of Michigan Comprehensive Cancer Center with recently published findings.

Methods: The authors searched a prospectively maintained melanoma database at the University of Michigan for patients with primary truncal melanoma who underwent lymphoscintigraphy and sentinel lymph node biopsy between 1997 and 2004. The association of MLBD with the clinical and pathologic characteristics collected and the presence of regional metastases was tested by using contingency tables and the {chi}2 test statistic and by using the Fisher’s exact test statistic when cell frequencies were small. The product-limit method of Kaplan and Meier was used to estimate disease-free and overall survival probabilities.

Results: Of 423 patients with primary truncal melanoma who underwent sentinel lymph node biopsy, 123 (29%) had a positive result, and 98 patients (23.2%) had MLBD. Patients with tumors located in the middle of the trunk and tumor ulceration were more likely to have MLBD (P < .0001 and P = .045, respectively). Patients with a single lymphatic drainage basin and MLBD had a similar risk of lymph node metastasis and similar disease-free and overall survival.

Conclusions: Patients with truncal melanomas tend to have MLBD when the tumor is located in the middle of the trunk or when ulceration is present. In our experience, drainage to multiple lymphatic basins was not an independent risk factor for sentinel lymph node metastasis and has no independent prognostic significance.

Key Words: Melanoma • Sentinel lymph node biopsy • Lymphoscintigraphy • Multiple basins


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Significant prognostic factors in patients with primary melanoma include Breslow thickness, tumor ulceration, and lymph node metastases. In patients with clinically negative lymph nodes, the presence of metastases in the sentinel lymph node (SLN) has been shown to be the strongest predictor for recurrence and survival.1,2 Intraoperative lymph node mapping and SLN biopsy have proven to be a reliable method for evaluating the status of regional lymph node basins, and this has become the standard approach in staging cutaneous melanoma patients at risk for lymph node metastasis.2 Melanomas located on the trunk, as compared with those located on the extremities, have also been associated with a worse prognosis, but the reasons for this remain unknown.3 As opposed to the extremities, melanomas on the trunk often drain to multiple lymphatic basins. As one would expect, truncal melanoma patients with clinical evidence of lymph node involvement in more than one lymphatic drainage basin have a worse prognosis than those with lymph node involvement of a single lymphatic drainage basin or no lymph node involvement at all.4,5 However, recent studies have suggested that multiple lymphatic basin drainage (MLBD) on lymphoscintigraphy, compared with drainage to just one basin, is independently associated with an increased risk of lymph node metastases6 or with a worse prognosis even with no pathologic lymph node involvement.7 Possible explanations for an increased risk of lymph node metastases proposed include the development of peritumoral collateral lymphatics secondary to paracrine effects or obstruction of existing lymphatic channels. Given the limited number of studies evaluating MLBD and its association with the incidence of SLN metastasis or prognosis and the inconsistent results, we retrospectively reviewed our experience with truncal melanomas and MLBD.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Approval of the study was obtained from the University of Michigan Institutional Review Board. Our prospective melanoma database was queried for patients with invasive melanoma of the trunk who underwent SLN biopsy. Between October 1997 and March 2004, 1152 patients underwent SLN mapping for cutaneous melanoma, of which 426 were located on the trunk. Melanomas located on any mucous membranes or genitalia or melanomas of the perineum and perianal regions were excluded. Of the 426 patients, 1 patient accounted for 2 primary truncal melanoma diagnoses, and the second diagnosis was excluded from this analysis. In addition, two patients were excluded because they had no SLN identified. Thus, 423 patients with a diagnosis of primary truncal melanoma who underwent SLN biopsy were evaluated and make up the study population (Table 1Go).


View this table:
[in this window]
[in a new window]
  		TABLE 1. Clinical and pathologic features of 423 patients with truncal melanomas
 
Clinical and pathologic data collected included age, sex, Breslow thickness (measured in millimeters), number of mitoses per square millimeter, and the presence or absence of angiolymphatic invasion, regression, satellitosis, ulceration, and neurotropism. Follow-up information from the date of definitive treatment was obtained from clinical chart review and from the University of Michigan Cancer Registry.

Intraoperative Lymph Node Mapping and SLN Biopsy Technique
Patients with lesions with a ≥1.0-mm Breslow depth, or <1.0 mm with other adverse features, are recommended for lymphatic mapping and SLN biopsy. Patients undergo same-day preoperative lymphoscintigraphy in which 99mTc sulfur colloid (CIS-US Inc., Bedford, MA) is injected intradermally around the primary lesion or biopsy site 2 to 4 hours before surgery to identify lymphatic basins and intransit nodes at risk. After induction of satisfactory anesthesia, isosulfan blue dye (Lymphazurin 1%; Hirsch Industries Inc., Richmond, VA) is injected intradermally around the primary lesion or biopsy site, and the area is massaged to promote lymphatic flow. After approximately 5 to 10 minutes, a hand-held gamma probe (Navigator GPS; US Surgical, Cincinnati, OH) is used to identify the area of maximal counts over the lymphatic basins identified by lymphoscintigraphy. A small incision is made directly overlying these hot spots and is carried down through the subcutaneous tissue into the node-bearing fat. Any blue, hot (defined as the hottest node and any other nodes within 10% of the counts per minute of the hottest node), or palpably suspicious lymph nodes are considered SLNs.

We defined MLBD as the identification of an SLN in more than one basin, with the basins defined as axillary, inguinal, or supraclavicular/cervical. In-transit nodes were not considered a separate basin. Patients who did not have an SLN identified were excluded from the study. Patients who had the suggestion of drainage to a second basin on lymphoscintigraphy, but did not have a SLN identified with the handheld gamma probe in the operating room, were labeled as having single lymphatic basin drainage.

Histopathologic Examination of SLNs
SLN specimens were fixed in 10% neutral buffered formalin, serially sectioned at 2 to 3 mm, and entirely embedded in paraffin. Hematoxylin and eosin staining was performed on two 5-µm sections from each tissue block. In addition, four unstained serial sections were prepared for possible future immunohistochemical analysis. If SLNs were negative by routine light microscopy, immunohistochemical staining was performed by using antibodies to the melanoma markers Melan-A (1/12.5 dilution; DAKO Corporation, Carpinteria, CA) and S-100 protein (1/500 dilution; DAKO).

Statistical Analysis
The event of interest in this population of truncal melanoma patients was defined as the occurrence of lymphatic drainage from the tumor site to more than one nodal basin (MLBD) during SLN biopsy. The association of MLBD with the clinical and pathologic characteristics collected (described previously) was tested by using contingency tables and the {chi}2 test statistic and by using the Fisher’s exact test statistic when cell frequencies were small. P values <.05 were considered significant in all analyses.

Clinical outcomes of interest included the presence of one of more positive SLNs upon lymphadenectomy, the time to disease recurrence, and the time to death. The univariate association of one or more metastatic SLNs with the clinical and pathologic features, including MLBD, was explored by using standard logistic regression techniques. The odds ratios, Wald-based P values, and 95% confidence intervals were calculated. A parsimonious multivariate model was constructed by using only the clinical and pathologic characteristics found to be at least marginally significantly associated in univariate analyses, defined as a P value <.10. A backward elimination algorithm was then used to eliminate nonsignificant characteristics until only significant characteristics remained. For time-to-event end points, time was calculated from the date of operation until the date of disease recurrence or death. Patients not experiencing either event were censored at the date of last clinical follow-up. The product-limit method of Kaplan and Meier was used to estimate disease-free (DFS) and overall survival (OS) probabilities. Parsimonious multivariate models were constructed by using Cox proportional hazards regression, by using the same backward elimination algorithm described previously. Hazard ratios and corresponding 95% confidence intervals are reported.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Clinical and Primary Tumor Characteristics and Associated SLN Findings
The clinical and primary tumor characteristics are listed in Table 2Go, along with their association with the likelihood of finding at least one positive SLN. Almost two thirds of the patients were male, and the median age was 50 years (range, 11–83 years). Overall, 123 patients (29%) had a positive SLN biopsy result.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Clinicopathologic characteristics of the patient population (N = 423) and the frequency of and univariate association with at least one positive sentinel lymph node (PSLN)
 
Drainage to more than one lymphatic basin (MLBD) was identified in 98 (23.2%) patients. The identification of MLBD was significantly associated with the location of the primary melanoma (Table 3Go). Patients with primary tumors located in the middle of the trunk were more likely to have MLBD (71.4%) than those with either right-sided (22.3%) or left-sided (20.7%) lesions (P < .0001). The only other factor significantly associated with drainage to more than one lymphatic basin was tumor ulceration. Patients whose tumors showed ulceration were more likely (P = .045) to have MLBD (30.6%) compared with patients without ulceration (20.9%). Age, sex, and other characteristics of the primary melanoma demonstrated no significant association with the likelihood of drainage to more than one basin.


View this table:
[in this window]
[in a new window]
  		TABLE 3. Clinicopathologic characteristics by the number of nodal drainage basins
 
Risk of Lymph Node Metastasis in Patients With Multiple Lymphatic Drainage Basins
The occurrence of at least one positive SLN was not significantly associated with the number of lymphatic drainage basins. Of patients with MLBD, 27 (27.6%) had at least 1 positive SLN, whereas of patients with a single lymphatic drainage basin, 96 (29.5%) had at least 1 positive SLN (P = .7). On univariate analysis, the occurrence of at least one positive SLN was significantly associated with younger age, increasing Breslow thickness, a mitotic rate greater than five mitoses per square millimeter, the presence of tumor ulceration, angiolymphatic invasion, and the absence of regression. However, on multivariate analysis, the presence of a positive SLN in patients with melanoma on the trunk was associated only with younger age (P < .0001), thicker lesions, and a mitotic rate greater than five mitoses per square millimeter (P = .04). This is identical to factors previously described by our institution.8

Association of the Number of Nodal Drainage Basins With DFS and OS
The median follow-up time calculated from the date of diagnosis to the last known contact date, regardless of intervening recurrence, was 2.7 years (range, .02–7.2 years). The median follow-up time was similar between patients with single lymphatic drainage basins and MLBD: 2.6 and 2.7 years, respectively. Two patients who had no follow-up information were excluded from survival analysis.

Among the 421 patients left for time-to-event endpoint analysis, 37 (8.7%) had disease recurrence, and 38 (9.0%) died (from any cause), with a total of 54 (12.8%) having either disease recurrence or death (from any cause) during follow-up. Twelve patients (3%) had a regional recurrence (five were regional only, and seven were combined regional and distant recurrences). DFS and OS were similar between patients with a single lymphatic drainage basin and MLBD. Figures 1Go and 2Go illustrate the Kaplan-Meier product-limit estimates for disease-free and OS, respectively, according to the number of nodal drainage basins. Log-rank test analyses indicate that DFS (P = .18) and OS (P = .32) were not statistically different in these two patient groups. Factors significantly associated with DFS and OS included Breslow depth, tumor ulceration, the presence of a positive SLN, angiolymphatic invasion (DFS only), and mitotic rate (DFS only). When adjusted for these tumor characteristics, the presence of MLBD demonstrated no significant association with DFS or OS.


Figure 1
View larger version (6K):
[in this window]
[in a new window]
  		FIG. 1. Kaplan-Meier product-limit estimates for disease-free survival based on the number of nodal drainage basins. Log-rank test analysis indicated that disease-free survival is not statistically different in these two patient groups (P = .18).

 

Figure 2
View larger version (6K):
[in this window]
[in a new window]
  		FIG. 2. Kaplan-Meier product-limit estimates for overall survival based on the number of nodal drainage basins. Log-rank test analysis indicated that overall survival is not statistically different in these two patient groups (P = .32).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Since the introduction of lymphoscintigraphy and SLN biopsy in the evaluation of patients with truncal melanoma, it has been recognized that lymphatic drainage patterns can be quite unpredictable.1,8–11 The original description of dermal lymphatic drainage was submitted in 1874 by Sappey,11 who described a line above the umbilicus that predicted cephalad or caudal drainage.12 This, along with the thought that lymphatic drainage tended to be ipsilateral, provided the framework for predicting lymphatic drainage through much of the 20th century.6 The unpredictability of dermal lymphatic drainage patterns has been demonstrated substantially over the last two decades and relates to both the location and number of lymphatic drainage basins.6–11,13–17

Studies of truncal melanoma patients undergoing preoperative lymphoscintigraphy have shown a wide range of patients with MLBD (5%–49%), with most recent studies reporting a range of 29% to 46%.6,7,13–17 In our analysis of 423 truncal melanoma patients, 23.2% had MLBD. Patient characteristics were largely similar between patients with single and double basin drainage. The most significant association with drainage to more than one lymphatic basin was the laterality of the melanoma. Patients with primary tumors located in the middle of the trunk were significantly more likely to have MLBD (71.4% vs. 22.3% for right-sided and 20.7% for left-sided tumors). This likely reflects a predictably higher number of tumors in the middle of the trunk with overlapping lymphatic drainage beds. In addition, patients with primary tumors exhibiting ulceration were also more likely to have MLBD. Possible explanations for this finding include inflammation-induced lymphangiogenesis via cytokines produced locally in response to the ulcer or some unknown lymphangiogenic stimulus produced by cells of this subset of melanomas. If true, this supports the idea that drainage to more than one lymphatic basin may be more than simply an anatomical phenomenon: it may also be related to the biology of the tumor (and host).

MLBD has variably been associated with an increased risk for SLN metastases and a poorer prognosis. Porter et al.6 first reported their experience of truncal melanomas with MLBD in 2000. They found that of 281 patients with truncal melanoma undergoing SLN biopsy, 31% had MLBD. Furthermore, they found that by multivariate analysis, MLBD was a risk factor for SLN metastasis (relative risk, 1.9; P = .03). Three follow-up studies of comparably sized cohorts, including this study, have not corroborated this finding (Table 4Go).7,13 In this study, we found similar numbers of SLN metastases in patients with single lymphatic drainage basins and MLBD (29.5% vs. 27.6%, respectively). In addition, with multivariate logistic regression analysis, the only factors associated with SLN metastasis were tumor thickness, mitotic rate, and patient age, similar to previous results from our group.14


View this table:
[in this window]
[in a new window]
  		TABLE 4. Studies of multiple lymphatic basin drainage in truncal melanomas
 
Jimenez et al.7 reported that MLBD was an independent predictor of decreased OS and relapse-free survival (both P = .04). This feature remained significant even among patients with negative SLNs (relative risk, 2.7; P = .03). In the present study, MLBD was not associated with decreased OS or DFS (P = .18 and .32, respectively). Although upon visual inspection of Fig. 1Go it appears as though there is some deviation of the curves for DFS, the smaller sample size translates to larger confidence intervals around the DFS point estimates. The confidence intervals for the single nodal basin and multiple nodal basin overlap, thus suggesting no clinically meaningful difference.

The difference in results may be a function of the patient population or SLN technique. In this population of patients with truncal melanoma, we found that 29% had positive nodes. This is slightly higher than some other reports,6,7 although it seems in line with other descriptions of melanomas on the trunk. In the Multicenter Selective Lymphadenectomy Trial I, a prospective multicenter trial of SLN biopsy in melanoma, truncal melanomas had a positivity rate of 27.2%.17 In the WHO-14 trial of elective versus therapeutic lymph node dissection, which was limited to melanomas of the trunk, the patients who underwent wide local excision alone had a nodal recurrence rate of 30%.18 It is possible that the Jimenez data, with a nodal positivity rate of 21%, represents a set of patients with a better prognosis, thus making a prognostic association with MLBD more significant.

Patients with melanoma on the trunk consistently demonstrate a worse prognosis than those with lesions on the extremities. The reasons for the poorer prognosis associated with a truncal location for cutaneous melanomas still remain to be demonstrated. Certainly, lymph node metastasis in more than one basin is a worse sign, because the number of involved lymph nodes (increased tumor burden) is strongly associated with outcome. Some authors have proposed that biologically worse melanomas may influence their drainage patterns, and, thus, melanomas found on lymphoscintigraphy to drain to multiple basins have a worse prognosis, regardless of whether lymph node metastases are identified on SLN biopsy. Possibly these tumors promote the development of collateral lymphatics that facilitate metastatic spread to more than one basin. This could be the result of compression of regional lymphatics by local tumor growth, congestion of primary drainage lymphatics by tumor cells, paracrine lymphangiogenic effects, or a combination of factors. This last theory has been proposed by Jimenez et al.7 as a possible explanation of their finding of decreased OS and relapse-free survival associated with MLBD. On review of our data, MLBD seems to be most strongly associated with tumor location, thus suggesting that this is primarily an anatomical issue. However, we also found that MLBD is significantly associated with tumor ulceration. It is feasible that there is some biologic factor that leads both to ulceration and to increased lymphatic drainage and that this portends a worse prognosis. In our experience, though, MLBD loses significance on multivariate analysis, where ulceration is significantly associated with DFS and OS.

In summary, MLBDs are identified in approximately 25% to 45% of patients with primary truncal melanoma. In this dataset, patients with truncal melanomas with ulceration or with melanomas located in the middle of the trunk tended to have MLBD more frequently. In our experience, drainage to multiple basins was not an independent risk factor for SLN metastasis and had no independent prognostic significance. Data from multiple centers, with longer follow-up, may be necessary to better determine the prognostic implications of drainage to multiple basins. Further study is necessary to identify features of truncal melanoma that explain its decreased survival compared with those lesions arising in the extremities.

Received for publication September 26, 2005. Accepted for publication February 20, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Gershenwald JE, Thompson W, Mansfield PF, et al. Multi-institutional melanoma lymphatic mapping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. J Clin Oncol 1999; 17:1–8.[Free Full Text]
  2. Johnson TM, Sondak VK, Bichakjian CK, Sabel MS. The role of sentinel lymph node biopsy for melanoma: evidence assessment 2005. J Am Acad Dermatol 2006;54(1):19–27.[CrossRef][Medline]
  3. Balch CM, Soong S, Ross MI, et al. Long-term results of a multi-institutional randomized trial comparing prognostic factors and surgical results for intermediate thickness melanomas (1.0 to 4.0 mm). Ann Surg Oncol 2000; 7:87–97.[Abstract]
  4. Barth RJ, Venzon DJ, Baker AR. The prognosis of melanoma patients with metastases to two or more lymph node areas. Ann Surg 1991; 214:125–30.[Medline]
  5. Coit DG, Rogatko A, Brennan MF. Prognostic factors in patients with melanoma metastatic to axillary or inguinal lymph nodes. Ann Surg 1991; 214:627–36.[Medline]
  6. Porter GA, Ross MI, Berman RS, et al. Significance of multiple nodal basin drainage in truncal melanoma patients undergoing sentinel lymph node biopsy. Ann Surg Oncol 2000; 7:256–61.[Abstract]
  7. Jimenez RE, Panageas K, Busam KJ, et al. Prognostic implications of multiple lymphatic basin drainage in patients with truncal melanoma. J Clin Oncol 2005; 23:518–24.[Abstract/Free Full Text]
  8. Thompson JF, Uren RF. Teaching points on lymphatic mapping for melanoma from the Sydney Melanoma Unit. Semin Oncol 2004; 31:349–56.[CrossRef][Medline]
  9. McMasters KM, Chao C, Wong SL, et al. Interval sentinel lymph nodes in melanoma. Arch Surg 2002; 137:543–7.[Abstract/Free Full Text]
  10. Uren RF, Howman-Giles R, Thompson JF, et al. Interval nodes: the forgotten sentinel nodes in patients with melanoma. Arch Surg 2000; 135:1168–72.[Abstract/Free Full Text]
  11. Sappey MPC. Anatomie, Physiologie, des Vaisseaux Lymphtiques Consideres Chez l’Homme et les Vertebras. Paris: De Lahaye Publishing 1874.
  12. Lock-Anderson J, Rossing N, Drzewiecki KT. Preoperative cutaneous lymphoscintigraphy in malignant melanoma. Cancer 1989; 63:77–82.[CrossRef][Medline]
  13. Jacobs IA, Chang CK, Salti GI. Significance of dual-basin drainage in patients with truncal melanoma undergoing sentinel lymph node biopsy. J Am Acad Dermatol 2003; 49:615–9.[CrossRef][Medline]
  14. Sondak VK, Taylor JM, Sabel MS, et al. Mitotic rate and younger age are predictors of sentinel lymph node positivity: lessons learned from the generation of a probabilistic model. Ann Surg Oncol 2004; 11:247–58.[Abstract/Free Full Text]
  15. Norman J, Wells K, Kearney R, et al. Identification of lymphatic drainage basins in patients with cutaneous melanoma. Semin Surg Oncol 1993; 9:224–7.[Medline]
  16. Berger DH, Feig BW, Podoloff D, et al. Lymphoscintigraphy as a predictor of lymphatic drainage from cutaneous melanoma. Ann Surg Oncol 1997; 4:13–8.[Medline]
  17. Morton DL, Thompson JF, Essner R, et al. Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: a multicenter trial. Multicenter selective lymphadenectomy trial group. Ann Surg 1999; 230:453–63.[CrossRef][Medline]
  18. Cascinelli N, Morabito A, Santinami M, et al. Immediate or delayed dissection of regional nodes in patients with melanoma of the trunk: a randomized trial. Lancet 1998; 351:793–6.[CrossRef][Medline]



This article has been cited by other articles:


Home page
 Arch SurgHome page
A. C. Federico, A. B. Chagpar, M. I. Ross, R. C. G. Martin, R. D. Noyes, J. S. Goydos, P. D. Beitsch, M. M. Urist, S. Ariyan, J. J. Sussman, et al.
Effect of Multiple-Nodal Basin Drainage on Cutaneous Melanoma
Arch Surg, July 1, 2008; 143(7): 632 - 638.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by McHugh, J. B.
Right arrow Articles by Sabel, M. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by McHugh, J. B.
Right arrow Articles by Sabel, M. S.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS