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Sentinel Lymph Node Biopsy for Head and Neck Melanomas

From the Division of Surgical Oncology (KMM, CC, SLW, MJE), James Graham Brown Cancer Center, the Division of Otolaryngology-Head and Neck Surgery (EL), and the Division of Plastic and Reconstructive Surgery (WKS), University of Louisville, Louisville, Kentucky; University of Texas M. D. Anderson Cancer Center (MIR), Houston, Texas; LDS Hospital (RDN), Salt Lake City, Utah; and the University of South Florida (DSR), Moffitt Cancer Center, Tampa, Florida.

Correspondence: Address correspondence and reprint requests to: Kelly M. McMasters, MD, PhD, Division of Surgical Oncology, University of Louisville-Brown Cancer Center, 315 East Broadway, Suite 309, Louisville, KY 40202; Fax: 502-629-3393; E-mail: kelly.mcmasters{at}nortonhealthcare.org

	ABSTRACT

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Background: Sentinel lymph node (SLN) biopsy for head and neck (H&N) melanomas may be more technically challenging compared with other locations because of complex lymphatic drainage patterns. This analysis was performed to compare the results of SLN biopsy for H&N, truncal, and extremity melanomas.

Methods: The Sunbelt Melanoma Trial includes patients aged 18 to 70 with melanomas 1.0 mm thick. Statistical comparison was performed by ² or analysis of variance test.

Results: A total of 2610 patients were evaluated with a median follow-up of 18 months. The mean number of SLN per nodal basin was 2.8, 2.7, and 2.1 for H&N, truncal, and extremity melanomas, respectively. Median Clark level, Breslow thickness, and percentage of ulceration were similar between the groups. Peri-parotid SLN was identified in 25% of cases; there were no facial nerve injuries. SLN biopsy for H&N melanoma had higher false-negative rates at 1.5% (vs. 0.5% for trunk or extremity) but less histologically positive SLN at 15% (vs. 23.4%, and 19.5%; P < .001) compared with truncal and extremity melanoma. Blue dye was visualized less frequently in SLN of H&N melanoma patients compared with those with trunk or extremity melanomas.

Conclusions: Preoperative lymphoscintigraphy and meticulous intraoperative search for blue/radioactive nodes may improve results in H&N melanomas.

Key Words: Head and neck melanoma • Sentinel lymph node • Recurrence • Lymphoscintigraphy • Nodal basins

	INTRODUCTION

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Melanomas of the head and neck (H&N) pose unique surgical challenges. The very rich and complex lymphatic and vascular drainage in this region of the body may account for the well known but not well-understood phenomenon: H&N melanomas are associated with increased likelihood of recurrence and diminished overall survival compared with other sites.¹

With the advent of lymphoscintigraphy, it became apparent that anatomic predictions of nodal drainage are not always reliable. This is especially true of H&N melanomas. Discordance between clinically predicted basins and actual drainage basins is commonly attributed to complex lymphatic drainage patterns.^2–5 We hypothesized that since sentinel lymph node (SLN) staging for H&N melanomas may be more challenging because of the variable lymphatic drainage, same-basin recurrence rates after a negative SLN biopsy (false-negative results) may be higher compared with melanomas in other sites. The purpose of this study was to compare SLN biopsy results and same-basin recurrence rates in H&N melanomas with those for truncal and extremity melanomas.

	METHODS

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The Sunbelt Melanoma Trial is a multi-institutional, prospective, randomized study approved by the Institutional Review Boards of the involved 79 centers in North America (Fig. 1). Patients enrolled between June 1997 and February 2002 were included in this study. Eligibility criteria included patient age 18 to 70 years with cutaneous melanomas 1.0 mm Breslow thickness and clinically negative (nonpalpable or N0) regional lymph nodes. Patients with more than one primary melanoma were excluded from the study, as were those who had already undergone wide local excision of the primary melanoma. Participating surgeons included predominantly surgical oncologists and general surgeons experienced with SLN biopsy for melanoma; a minority of surgeons specialized in head and neck surgery or plastic surgery.

View larger version (27K): [in this window] [in a new window]   FIG. 1. The Sunbelt Melanoma Trial schema. LN, lymph node; PCR, polymerase chain reaction; Intron A, interferon alfa-2b adjuvant therapy.

Nodal basins were defined as follows: axillary, inguinal, epitrochlear, popliteal, or cervical. The cervical nodal basin was further subdivided into anterior cervical, posterior cervical, submental, supraclavicular, and parotid compartments. Note was also made of ectopic or in-transit SLN locations.

SLN were processed by conventional hematoxylin and eosin (H&E) staining at multiple levels, with at least five sections per block, along with two additional random sections for immunohistochemistry (IHC) of S100 protein. In addition, IHC for HMB-45, MART-1, or other markers was performed in a small number of centers. A central pathology review committee evaluated the first 10 cases from each participating institution, as well as all cases of SLN metastasis.

Patients found to have a SLN with metastatic disease by H&E staining and/or IHC underwent completion lymph node dissection of the involved nodal basin(s). Nonsentinel nodes were evaluated by routine H&E staining (not by serial sectioning or IHC). Complications were specifically evaluated using standardized case report forms filled out at each follow-up visit. Sensory and motor nerve complications were evaluated by both subjective patient complaints and physical findings, although detailed pre- and postoperative neurologic testing or questionnaires were not performed routinely.

Statistical comparison was performed using Pearson’s ² analysis, Fisher’s exact test, or analysis of variance, as appropriate. Significance was determined at P < .05. Data from all 2610 patients were included in all analyses, except in analysis of the proportion of patients with positive SLN, in which only those with complete histology and IHC data were included. Although complete data from all patients was not universally available, we decided to be inclusive rather than exclusive in the analysis of data and not to exclude patients from the analysis.

	RESULTS

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A total of 2610 patients were included in this study. Median follow-up was 18 months. The clinicopathologic characteristics of patients by primary melanoma site are shown in Table 1. H&N melanoma demonstrated male predominance compared with melanomas of the trunk or extremity (71% vs. 67% and 42%, respectively; P < .001) and a lower incidence of regression (5% vs. 16% and 8%, respectively; P < .001). H&N melanomas were more commonly desmoplastic compared with melanomas of the trunk and extremity (4% vs. 1.4% and 2.2%, respectively; P = .03). However, there were no significant differences in the other prognostic factors listed in Table 1.

As shown in Table 2, the average number of sentinel lymph nodes harvested per basin was 2.83, 2.72, and 2.14 in the H&N, truncal, and extremity sites, respectively (P < .0001). Of the H&N melanoma patients who received blue dye injection, only 59% of the SLN identified were stained blue, significantly less than that seen in the trunk and extremity melanoma patients (68.6% and 74%, respectively; P < .001). H&N melanoma patients also had a significantly lower incidence of SLN metastasis (detected by either H&E or IHC) compared with truncal and extremity melanomas (15% vs. 23% and 20%, respectively; P < .01). There was no significant difference in the frequency of IHC-only detected SLN metastases among the H&N, trunk, and extremity melanoma location groups. All IHC-only positive SLNs were S100 positive; no patient had a diagnosis of an IHC-positive SLN solely based on markers other than S-100.

There were no significant differences in Breslow thickness among the H&N, truncal, or extremity melanoma patients when patients with or without recurrence were considered (Table 3). Furthermore, there were no significant differences in other major prognostic factors such as Clark’s level, ulceration, and lymphovascular invasion among H&N, trunk, and extremity melanoma patients who developed recurrence (data not shown).

	DISCUSSION

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Melanomas of the H&N do not always follow clinically or anatomically predictable patterns of metastasis due to multiple overlapping lymphatics and complex drainage patterns.^2–5 With lymphatic mapping and SLN biopsy, however, these drainage patterns can be discerned. SLN biopsy is also a more technically demanding procedure to perform in the H&N region because multiple small SLN are often encountered and dissection of lymph nodes located in the parotid gland region presents special challenges, specifically the risk of facial nerve injury.^3,14–17 Our series noted that one quarter of the SLN harvested drained to the peri-parotid region, exactly consistent with Carlson’s series,¹⁵ whereas others have reported an incidence of up to one third³ and one half¹⁶ of patients. Although 1.6% of all the complications in H&N melanomas were motor nerve paresis (Table 6), two of the injuries occurred secondary to completion lymph node dissection. There were no facial nerve injuries due to a sentinel lymphenectomy in the peri-parotid region. Two patients had spinal accessory nerve weakness as a result of SLN biopsy of the neck.

While multiple basins are common in the H&N primary, in this series, truncal melanomas had 1 basin mapped more frequently (28.3%) than either H&N (17.3%; P < .001) or extremity (5.3%; P < .001). The incidence of contralateral basin identification was 6.5% in our study, whereas the literature cites that as high as 10% of patients may have such drainage patterns.⁴ In our study, only 59% of the SLN were stained blue, among the patients injected with blue dye, (Table 2) compared with 67% for trunk and 74% for extremity melanomas. This result may be attributed to the empiric observation that the blue dye washes out more quickly in the H&N location, perhaps due to its abundant vascularity, compared with other sites of the body.¹⁸ Using a 1:3 ratio of radiocolloid and isosulfan blue dye, Bostick reported that 91% of harvested SLN were blue.¹⁹ In his series, the incision and search for the SLN ensued within 3 to 5 minutes of the blue dye injection coupled with repeated dye injections every 20 minutes as necessary. Although the time to incision after injection of blue dye was not recorded in our study, it is likely to have been longer than in Bostick’s study. The lower incidence of blue dye staining and SLN metastasis in H&N melanomas is despite the fact that, on average, 2.83 SLNs per patient were harvested, more than for any other primary site.

Our study had a 97% SLN identification rate for H&N melanomas. This is a higher rate than other reported rates where up to 10% of H&N melanoma patients may not have identifiable SLN.²⁰

Finally, the incidence of same basin recurrences (false-negative results) has ranged from 0% in two studies,^18,19 with a median follow-up of 11.6 and 46 months, respectively, to 10.5%²⁰ with a mean follow-up of 23 months; and as high as 25% within 12 months as reported by O’Brien from the Sydney Melanoma Unit.³ In our study, the incidence of false-negative results was 1.9% with a median follow-up of 18 months. This was significantly higher than the incidence of false-negative results seen in trunk and extremity melanomas (0.5% each; P < .05). Technical variations, differing types of radioactive colloid, and differences in the follow-up period in these studies may explain, in part, the differences in results. The relatively short follow-up period in the present study also must be considered, and the differences in the false-negative rate may become more pronounced with further follow-up.

The increased frequency of same-basin recurrences and the significantly lower incidence of nodal metastasis detected in H&N melanoma may indicate that SLN biopsy for H&N melanomas is less reliable and technically more challenging than for melanomas in other locations. In the present study, although the incidence of same-basin recurrences was slightly greater for H&N melanomas versus other locations, the degree of accuracy of nodal staging for H&N melanomas is acceptable. The overall morbidity for SLN biopsy in H&N melanoma is relatively low. However, the relative benefit of a minimally invasive procedure has to be balanced with the false-negative rate. Further follow-up is necessary to establish the long-term false-negative rate for H&N melanomas in multi-institutional practice. It is also possible that standard histopathological techniques for analyzing the SLN are inadequate for accurate staging, especially for H&N melanomas. Ultra-sensitive molecular staging methods such as reverse transcription-polymerase chain reaction, may provide more accurate prognostication. The results of the Sunbelt Melanoma Trial, which evaluates the clinical significance of molecularly detected micrometastatic disease, are therefore of critical interest and clinical importance.^21,22

This study underscores the importance of attention to the technical aspects of SLN biopsy in H&N melanomas: detailed preoperative lymphoscintigraphy, prompt search for blue nodes, and thorough knowledge of the anatomy of the region. Such technical factors are likely to improve the results of SLN staging of H&N melanomas.

	CONCLUSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Lymphatic mapping can guide the decision to dissect a particular nodal basin in H&N melanomas. H&N melanomas are associated with a lower rate of positive SLN, even though most primary tumor prognostic factors (i.e., Breslow thickness and ulceration) are not different compared with truncal and extremity melanomas. SLN from patients with H&N melanomas are less likely to contain visible blue dye staining. H&N melanomas are associated with a slightly greater risk of false-negative results, despite removal of a greater number of SLN. Detailed preoperative lymphoscintigraphy and meticulous intraoperative search for blue/radioactive nodes may improve results.

APPENDIX
I: Sunbelt Melanoma Trial Investigators
Stephan Ariyan, MD, Yale University, New Haven, CT; Frederick Aronson, MD, Maine Center for Cancer Care, Scarborough, ME; Michael B. Atkins, MD, Beth Israel Deaconess Medical Center, Boston, MA; Bruce Averbook, MD, Metro Health Medical Center, Cleveland, OH; Paul Baron, MD, Roper Hospital, Charleston, SC; Mansoor H. Beg, MD, North Shore University Hospital, Great Neck, NY; Peter D. Beitsch, MD, Dallas Surgical Group (St. Paul Med), Dallas, TX; John L. Bell, MD, UT Medical Center, Knoxville, TN; Marc Boisvert, MD, Washington Cancer Institute, Washington, DC; Richard A. Bold, MD, UC Davis Cancer Center, Sacramento, CA; Ralph Broadwater, MD, Arkansas Cancer Research Center, Little Rock, AR; Ned Z. Carp, MD, Lankenau Hospital, Wynnewood, PA; A. Lawrence Cervino, MD, Summa Health Systems/Akron, Akron, OH; David Z.J. Chu, MD, City of Hope National Center, Duarte, CA; Rosa Cuenca, MD, East Carolina University, Greenville, NC; Paul S. Dale, MD, Southeastern Surgical Oncologists, Macon, GA; George W, Daneker, MD, Northside Hospital - Atlanta Regional CCOP, Atlanta, GA; Scott Davidson, MD, Cancer Center at Providence Hospital, Mobile, AL; Bradley Scott Davidson, MD, 5 Mobile Infirmary Medical Center, Mobile, AL; Marie France Demierre, MD, Boston Medical, Boston, MA; Mukund S. Didolkar, MD, Sinai Hospital of Baltimore, Baltimore, MD; Raza Dilawari, MD, Methodist Hospitals of Memphis (Boston Baskin), Memphis,TN; Larry Dillon, MD, Memorial Hospital Colorado Springs, Colorado Springs, CO; Paul S. Dudrik, MD, UT Medical Center, Knoxville, TN; David Dunning, MD, Northern Virginia Oncology Group, PC, Fairfax, VA; J. Benton Dupont, MD, Baton Rouge General Medical Center, Baton Rouge, LA; Burton L. Eisenberg, MD, Fox Chase Cancer Center, Philadelphia, PA; Robert K. Finley, III, MD, Dayton Clinical Oncology Program, Dayton, OH; Thomas G. Frazier, MD, Bryn Mawr Hospital, Bryn Mawr, PA; Michele Gadd, MD, Massachusetts General Hospital, Boston, MA; Charles E. Geyer, JR, MD, Joe Arrington Cancer Center, Lubbock, TX; W. Larry Gluck, MD, Cancer Centers of the Carolinas, Greenville, SC; James S. Goydos, MD, Cancer Institute of New Jersey, New Brunswick, NJ; Keith Heaton, MD, Park Nicollet Clinic/HealthSystem Minnesota, St. Louis Park, MN; Richard A. Hoefer, JR, DO, FACS, Oyster Point Surgical Associates, PC, Newport News, VA; Ryan F. Holbrook, MD, Sacred Heart Med Center/Deaconess Med Center, Spokane, WA; Lisa Jacobs, MD, University of Missouri Ellis Fischel Cancer Center, Columbia, MO; William Jewell, MD, Kansas University Research Institute, Kansas City, KS; Peter Jochimsen, MD, University of Iowa, Iowa City, IA; Denise L. Johnson, MD, Stanford University Medical Center, Stanford, CA: Richard Keidan, MD, William Beaumont Hospital, Royal Oak, MI; Mark C. Kelley, MD, Vanderbilt University Medical Center, Nashville, TN; V. Suzanne Klimberg, MD, Arkansas Cancer Research Center, Little Rock, AR; Mark Kozloff, MD, Ingalls Hospital, Harvey, IL; William G. Kraybill, MD, Roswell Park Cancer Institute, Buffalo, NY; Joseph A. Kuhn, MD, Baylor University Medical Center, Dallas, TX; Jeffrey E. Lee, MD, M.D. Anderson Cancer Center, Houston, TX; D. Scott Lind, MD, University of Florida College of Medicine, Gainesville, FL; Paul F. Mansfield, MD, M.D. Anderson Cancer Center, Houston, TX; Kelly Marc McMasters, MD, University of Louisville, Louisville, KY; Greg P. Midis, MD, UT Medical Center, Knoxville, TN; Richard C. Montgomery, MD, Lexington Clinic/St. Joseph Hospital, Lexington, KY; Michael Nolen, MD, O U C M -T, Tulsa, OK; James H. North, MD, Eisenhower Army Med Center, Fort Gordon, GA; R. Dirk, Noyes, MD, LDS Hospital, Salt Lake City, UT; Thomas Olencki, D.O., The Cleveland Clinic Foundation, Cleveland, OH; Steven Pandelidis, MD, York Hospital/PA, York, PA; David B. Pearlstone, MD, Cancer Centers of the Carolinas, Greenville, SC; Roger R. Perry, MD, Sentara Cancer Institute/EVMS, Norfolk, VA; E. Phillip Polack, MD, Wheeling Hospital West Virginia, Wheeling, WV; Maurice Rawlings, Jr., MD, Memorial Hospital, Chattanooga, TN; Douglas Reintgen, MD, Moffitt Cancer Center, Tampa, FL; Calvin Ridgeway, MD, Albuquerque Surgical Group, PA, Albuquerque, NM; Lee B. Riley, MD, PhD, St. Luke’s Hospital, Bethlehem, PA; David C. Ritter, MD, Lee Memorial Cancer Center, Naples, FL; Catherine Ronaghan, MD, Joe Arrington Cancer Center, Lubbock, TX; Merrick I. Ross, MD, M.D. Anderson Cancer Center, Houston, TX; Elizabeth Saettler, MD, CancerCare/Manitoba, Winnipeg Manitoba, Canada; Armando Sardi, MD, St. Agnes Healthcare, Baltimore, MD; Donna Schade, MD, M.D. Anderson Cancer Center Orlando, Orlando, FL; Elin R. Sigurdson MD, Fox Chase Cancer Center, Philadelphia, PA: David A. Sloan, MD, University of Kentucky, Lexington, KY; Jeffrey Sussman, MD, University of Cincinnati, Cincinnati, OH; Kenneth K. Tanabe, MD, Massachusetts General Hospital, Boston, MA; Peter Tate, MD, Central Baptist Hospital, Lexington, KY; Clifford Thompson, MD, Mima Century Research Associates, Melbourne, FL; Roderick Tompkins, MD, Kings Daughters - Ashland, Ashland, KY; Courtney M. Townsend, Jr., MD, University of Texas Med Br/Galveston, Galveston, TX; Douglas Tyler, MD, Duke University Medical Center, Durham, NC; Marshall M. Urist, MD, University of Alabama - Birmingham, Birmingham, AL; Charles N. Verheyden, MD, PhD, Scott and White Memorial Hospital - Texas, Temple, TX; Richard L. White, Jr., MD, Carolinas Medical Center, Charlotte, NC

	Acknowledgments

 
This study was supported by a grant from Schering Oncology-Biotech and the Center for Advanced Surgical Technologies (CAST) of Norton Hospital, Louisville, KY. The authors thank Deborah Hulsewede, Debra Williams, Sherri Matthews, and Diana Simpson for their continued dedication to the data management and coordination of this study, and Susan Kemper for her expert manuscript preparation. The authors are also grateful to all members of the Sunbelt study group for their continued participation.

	Footnotes

 
Presented at the Society of Surgical Oncology Annual Meeting, Denver, CO, March 14–17, 2002.

SLN biopsy for H&N melanomas may represent a unique challenge because of complex lymphatic drainage patterns. H&N melanomas are associated with a slightly greater risk of false negative results.

Received for publication June 6, 2002. Accepted for publication September 6, 2002.

	REFERENCES

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