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10.1245/s10434-007-9412-x
Annals of Surgical Oncology 14:1890-1895 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Axillary Reverse Mapping (ARM): A New Concept to Identify and Enhance Lymphatic Preservation

Margaret Thompson, MD1, Soheila Korourian, MD2, Ronda Henry-Tillman, MD1, Laura Adkins, MAP1, Sheilah Mumford, MA1, Kent C. Westbrook, MD1 and V Suzanne Klimberg, MD1,2

1 Division of Breast Surgical Oncology, Department of Surgery, University of Arkansas for Medical Sciences, Little Rock, AR, USA
2 Department of Pathology, University of Arkansas for Medical Sciences, Little Rock, AR, USA

Correspondence: Address correspondence and reprint requests to: V Suzanne Klimberg, MD; E-mail: klimbergsuzanne{at}uams.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Variations in arm lymphatic drainage put the arm lymphatics at risk for disruption during axillary lymph node surgery. Mapping the drainage of the arm with blue dye (axillary reverse mapping, ARM) decreases the likelihood of disruption of lymphatics and subsequent lymphedema.

Methods: This institutional review board (IRB)-approved study from May to October 2006 involved patients undergoing SLNB and/or ALND. Technetium sulfur colloid (4 mL) was injected in the subareolar plexus and 2–5 mL of blue dye intradermally was injected in the ipsilateral upper extremity (ARM). Data were collected on variations in lymphatic drainage that impacted SLNB or ALND, successful identification and protection of the arm lymphatics, any crossover between a hot breast node and a blue arm node, and occurrence of lymphedema.

Results: Of the 40 patients undergoing surgery for breast cancer, 18 required an ALND, with a median age of 49.7 years old. Fourteen patients had a SLNB + ALND, and four patients had ALND alone. In 100% of patients, all breast SLNs were hot but not blue, and the false negative rate was 0. In 11 of 18 ALNDs (61%) blue lymphatics or blue nodes were identified in the axilla. In the initial seven cases with positive lymph nodes in the axilla, the blue node draining from the arm was biopsied and all were negative.

Conclusions: ARM identified significant lymphatic variations draining the upper extremities and facilitated preservation in all but one case. ARM added to present-day ALND and SLNB further defines the axilla and may be useful to prevent lymphedema.

Key Words: SLNB • ALND • Lymphedema


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The morbidity and risks of an axillary lymph node resection (ALND) include the risk of general anesthesia, permanent hypesthesia, and/or dysesthesia at the posterior aspect of the arm1,2 painful neuroma, postoperative seroma formation;3 perhaps the most long-term and devastating is lymphedema of the arm.1 Depending on the definition and extent of axillary dissection, lymphedema alone remains 5–15%, but has been reported as high as ~77% (Table 1Go).4–11 Subsequent associated psychological distress ranges from 17–50%.12,13 Sentinel lymph node biopsy (SLNB) was introduced and designed to prevent lymphedema. However, recent short-term studies demonstrate that even with SLNB alone lymphedema rates range 2–7%.4,14,15 Further, with a positive SLNB, an axillary node dissection is still the standard of care.


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  		TABLE 1. Lymphedema in ALND Vs SLNB
 
We hypothesized that the virtually unknown variations in arm lymphatic drainage put the arm lymphatics at risk for disruption during ALND and to a lesser degree SLNB. Therefore, mapping the drainage of the arm with blue dye and preserving the identified lymphatics would decrease the likelihood of disruption of the lymphatics draining the arm during ALND or SLNB. We have termed this new procedure axillary reverse mapping (ARM) because we are identifying that which we wish to preserve. This is the reverse of the SLNB where we seek to identify that which we seek to remove. This paper reports the development and initial results of the ARM procedure.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
This institutional review board (IRB)-approved, prospective, nonrandomized study involved patients with pathologically proven breast cancer undergoing SLNB and/or ALND. Consecutive patients were scheduled to have an ALND alone, or in conjunction with a partial mastectomy, a total mastectomy, or a positive SLNB. ALND involved resection of level I and II nodes, and if indicated for palpable disease, level III nodes.

SLNB Procedure
At our institution, we perform intraoperative injection of technetium, as previously described in detail.16 Briefly, under general anesthesia, 1.0 mCi of unfiltered technetium sulfur colloid, diluted to a final volume of 4.0 mL or less with saline was injected in the subareolar lymphatic plexus by inserting the needle at the limbus of the areola at 45° to instill just beneath the nipple.9 Routine scrub, prep, and drape were then completed. Radioactivity counts in the axilla were recorded prior to the incision. The hand-held gamma probe (Neoprobe, Dublin, OH) was used to localize radioactivity. If the radioactive SLN could not be located prior to the incision via gamma probe, then the blue dye (Isosulfan) was injected in the breast in the subareolar plexus. All hot and palpable nodes were submitted for pathology as SLNs. Patients then underwent excision of the tumor via lumpectomy or mastectomy. Dissection of the axilla was performed if SLNs were positive.

ARM Procedure
In the developed technique, 2.5 mL of Lymphazurin was injected dermally or subcutaneously in the upper inner arm along the medial intramuscular groove of the ipsilateral arm in order to locate the draining lymphatics from the arm (Fig. 1Go). In the first few patients, the blue dye was injected in the dorsum of the hand or posterior arm. The upper, inner areas was chosen simply because it had the most rapid drainage and it also hid the tattoo that could last anywhere from 1 week to 6 months. After injection, the site was massaged and the arm elevated for 5 minutes to enhance arm lymphatic drainage. We then proceeded as usual with the SLNB or ALND. After dissection through the axillary fascia, we noted any blue dye and/or blue lymphatics. In the first few patients, we did take the blue node to confirm no cancer cells were in them even when the axilla had many positive nodes. Later, knowing these were draining the arm and not the breast, they were identified and preserved.


Figure 1
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  		FIG. 1. Palpation of the upper, inner ipsilateral arm locates the intramuscular groove where the blue dye is injected dermally or subcutaneously.

 
ALND
For the ALND, the incision was made in the usual fashion; unless a mastectomy was done at the same time then the ALND was performed through the mastectomy incision. Once through the axillary fascia, the anterior border of the pectoralis minor muscle was opened. The anterior border of the latissimus muscle was also opened and carried superiorly to its tendinous insertion. The axillary vein was identified and preserved. The axillary fat pad was cleared from the axillary vein using sharp dissection, and then bluntly dissected in an inferior fashion. This allowed identification of the thoracodorsal bundle and the long thoracic nerve, which were preserved. After the first seven cases, blue lymphatics and blue nodes were protected. The axillary contents were then removed with sharp dissection and sent to pathology. All wounds were closed after placing a drain.

Pathology
In the first few cases where we did take the blue nodes, they were labeled as blue arm node. If they were greater than 5 mm, they were sectioned in 3-mm intervals along the long axis. The breast SLNs greater than 5 mm in size were sectioned at 3-mm intervals along the long axis. Intraoperative touch prep cytology was performed followed by routine hematoxylin and eosin staining. Complete axillary dissection specimens were submitted for pathology as axillary contents. The axillary lymph nodes were bisected along the long axis and 1 section from each node was submitted for hematoxylin and eosin staining.

Study Objectives and Statistics
Data were collected on variations in lymphatic drainage that impacted SLNB or ALND, successful protection of the arm lymphatics, successful identification of breast SLNB, any crossover between a hot breast node and a blue arm node, and occurrence and prevention of lymphedema. Descriptive statistics were used to calculate the mean and standard deviation.17


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patients
From May 12, 2006 to October 1, 2006, 40 patients were enrolled in this study, with 10 undergoing bilateral mastectomies, making a total of 50 ARM procedures. Of the 50 ARM procedures, 32 were in SLNB, 4 ALND, and 14 SLNB+ALND. Of those patients undergoing ARM and ALND, the median age of patients was 49.7 years old (range 26–69, SD 13 years old). All 18 (100%) ALND were performed in patients who had invasive breast cancer on initial biopsy, with three having inflammatory breast cancer, one having recurrent breast cancer, and one patient with bilateral breast cancer. Surgeries included five (28%) partial mastectomies (PM), 10 (56%) mastectomies (Mast), one (5%) wide chest wall excision, and two (11%) ALND alone (Table 2Go).


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  		TABLE 2. Patient characteristics
 
Surgery
Eleven of 18 (61%) blue lymphatics and/or blue nodes were identified in the axilla proper (Fig. 2Go). In five cases, blue lymphatics were identified. In three cases, blue nodes were identified. In three cases, blue lymphatics and blue nodes were identified. In seven cases, no blue lymphatics or nodes were identified. There were variations in the location of blue lymphatics: above and below but near the vein, adjacent to the SLN, or draped over the SLN. The blue nodes were never hot. In the initial seven cases, the blue lymph nodes were biopsied and were never positive when breast hot nodes were positive with breast cancer. In two cases, the blue node was identified but attached to a 6-mm blue lymphatic and left intact. In one case, the blue lymphatic went into matted nodes and was sacrificed followed by immediate postoperative lymphedema (Table 3Go). In the remaining 32 SLNB cases there was complete non-concordance. That is SLNB were never blue and ARM nodes were never hot.


Figure 2
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  		FIG. 2. Blue lymphatics and/or blue nodes identified in the axilla from three different patients.

 

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  		TABLE 3. ARM procedure
 
Pathology
The average number of lymph nodes taken during the ALND was 12.5 (range 3–21, SD 5). All blue nodes identified and sent separately to pathology were negative. Complete axillary dissection revealed an average of 3.3 positive lymph nodes (range 0–15, SD 4).

Complications
One patient experienced a localized skin reaction at the site injection. There were no systemic allergic reactions. Most patients experienced a temporary blue tattoo at the injection site, which lasted anywhere from a few days to a 6 months. One case of lymphedema developed in the patient where a 6-mm blue lymphatic was sacrificed as it was matted with her grossly positive axillary nodes.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The status of the regional lymph node(s) is the key prognostic variable on which therapeutic decisions are based dependent on the presence or absence of breast cancer cells metastatic to the axillary lymph node(s).18 The results of randomized prospective clinical trials, which guide current therapy, have been based on the pathologic status of the axillary lymph nodes.19 The National Cancer Institute’s consensus statement regarding breast cancer was based, in part, on the pathologic status of lymph nodes.20 Although newer markers of oncogene expression show promise with respect to treatment of breast cancer, the status of the axillary nodes remains the most important prognostic criteria and will continue to have direct impact on clinical decisions.21

Annually, an enormous number of women undergo staging axillary lymph node resections in the United States. This operation is generally performed on all women with operable breast cancer in whom adjuvant therapy will be considered if the lymph nodes are positive for metastatic cancer cells. In 2006, more than 212,000 women were diagnosed with breast cancer.22 Analysis of cases recorded in the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute23 and data from the Commission on Cancer of the American College of Surgeons indicate that approximately 89% of these women had surgery that involved resection of the axillary lymph nodes. Thus, approximately 161,000 women with breast cancer will undergo some resection of axillary lymph nodes. The technique of axillary lymph node dissection has changed little over several decades. The principal features of resection are removal of axillary tissue inferior to the axillary vein, lateral to the serratus anterior and anterior to the teres major and medial to the latissimus dorsi.24 Lymphedema remains the most published complication from an ALND.5,12,13,25–32 Lymphedema in patients undergoing ALND ranges from 13–52% varying with the definition and method to determine lymphedema, length of follow-up,33 number of positive lymph nodes, postoperative irradiation, and body habitus.34

Sentinel lymph node biopsy (SLNB) was developed to prevent the high morbidity seen with ALND (Table 1Go). The SLN is the first draining lymph node from the primary breast cancer. Radioactivity and/or blue dye is injected into the breast and drains to the SLN. Many studies have shown the SLN status to be reflective of that of the axilla.35–38 From its inception, SLNB has been assumed to be less morbid, but until recently, few objective data existed. Because of the long-term consequences of lymphedema, its end result is an essential measurement when SLNB is evaluated. In the American College of Surgeons Oncology Group Z0010 prospective observational study,15 2904 patients had arm circumference measured before surgery and again 6 months after surgery. Seven percent of the patients had lymphedema defined as a change in arm circumference >2 cm when compared to the contra-lateral or control arm and baseline measurements. Although multiple comparison studies have confirmed that SLNB consistently has lower morbidity and lymphedema rates than ALND; it is still clinically significant ranging from 0–13% (Table 1Go).

Prevention is of key importance to avoid lymphedema formation.39 The goal of the ARM pilot study was to develop a technique to identify and preserve arm lymphatic drainage, thus decreasing the occurrence of lymphedema associated with staging the axillary lymph nodes in patients with breast cancer. This report describes the first effort in which blue dye is injected into the ipsilateral arm of the ALND to map arm lymphatics. Injection anywhere in the arm worked well; the upper, inner areas was chosen simply because it had the most rapid drainage and it also hid the tattoo that could last anywhere from 1 week to 6 months. The proof of this principle comes from many SLNB done for arm melanoma.40 We found that injecting 2.5–5 mL of blue dye resulted in successful identification of blue lymphatics/nodes within the axilla proper in 61% of cases in our first 18 ALNDs. There was nonconcordance of arm and breast lymphatic drainage even in heavily positive axillas.

There were clinically significant lymphatic variations that ARM identified and allowed preservation in all but one case. Arm lymphatics are generally described just below or around the vein, and for that reason skeletonizing the axillary vein is avoided. We found about one-third of these blue lymphatics can be significantly below the vein, even 3–4 cm. Prior to our use of the ARM technique, we certainly would have sacrificed a good number of these now easily identifiable arm lymphatics, not realizing that they were draining the arm and not the breast. Likewise, approximately one-third of the SLNB cases confirmed these low-lying ARM lymphatics. ARM lymphatics were identified juxtaposed to and even overlapping the SLN in some cases—identifying a potential cause of lymphedema after SLNB.

Success of this technique in preventing lymphedema will require ongoing follow-up and studies. We currently have a prospective study that will measure arm volume. At present the longest follow-up is 8 months. None of the patients where the ARM lymphatics were identified and preserved have developed lymphedema.

This ARM technique demonstrated significant variation in the arm lymphatics, allowed identification of these lymphatics and subsequent preservation, and fortuitously suggests that there does not appear to be cross talk between arm lymph node and breast lymph node drainage. By identifying and preserving the arm lymphatics during ALND and even SLNB, this technique may prevent most lymphedema.


   FOOTNOTES
 
Supported by the Susan G. Komen Breast Cancer Clinical Fellowship and the Arkansas Breast Cancer Act

Received for publication February 14, 2007. Accepted for publication March 7, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Ivens D, et al. Assessment of morbidity from complete axillary dissection. Br J Cancer 1997; 66:136.
  2. Temple LK, Baron R, Cody HS 3rd, et al. Sensory morbidity after sentinel lymph node biopsy and axillary dissection: a prospective study of 233 women. Ann Surg Oncol 2002; 9(7):654–62.[Abstract/Free Full Text]
  3. Somers RG, et al. The use of closed suction drainage after lumpectomy and axillary node dissection for breast cancer; a prospective randomized trial. Ann Surg 1992; 215:146.[Medline]
  4. Schrenk P, Rieger R, Shamiyeh A, et al. Morbidity following sentinel lymph node biopsy versus axillary lymph node dissection for patients with breast carcinoma. Cancer 2000; 88:608–14.[CrossRef][Medline]
  5. Haid A, Koberle-Wuhrer R, Knauer M, Burtscher J, Fritzsche H, Peschina W, Jasarevic Z, Ammann M, Hergan K, Sturn H, Zimmermann G. Morbidity of breast cancer patients following complete axillary dissection or sentinel node biopsy only: a comparative evaluation. Breast Cancer Res Treat 2002; 73(1):31–6.[CrossRef][Medline]
  6. Swenson KK, Nissen MJ, Ceronsky C, Swenson L, Lee MW, Tuttle TM. Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol 2002; 9(8):745–53.[Abstract/Free Full Text]
  7. Blanchard DK, Donohue JH, Reynolds C, et al. Relapse and morbidity in patients undergoing sentinel lymph node biopsy alone or with axillary dissection for breast cancer. Arch Surg 2003; 138:482–8.[Abstract/Free Full Text]
  8. Schijven MP, Vingerhoets AJ, Rutten HJ, et al. Comparison of morbidity between axillary lymph node dissection and sentinel node biopsy. Eur J Surg Oncol 2003; 29:341–50.[CrossRef][Medline]
  9. Ronka R, von Smitten K, Tasmuth, et al. One-year morbidity after sentinel node biopsy and breast surgery. Breast 2005; 14:28–36.[CrossRef][Medline]
  10. Leidenius M, Leivonen M, Vironen J, von Smitten K. The consequences of long-time arm morbidity in node-negative breast cancer patients with sentinel node biopsy or axillary clearance. J Surg Oncol 2005; 92(1):23–31.[CrossRef][Medline]
  11. Mansel R, Fallowfield L, Kissin M, et al. Randomized multi-center trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: The ALMANAC Trial:. JNCI 2006; 98(9):599–609.[Abstract/Free Full Text]
  12. Passik SD, McDonald MV. Psychosocial aspects of upper extremity lymphedema in women treated for breast carcinoma. Cancer 1998; 83:2817–20.[CrossRef][Medline]
  13. Tobin MB, Lacey HJ, Meyer L, Mortimer PS. The psychosocial morbidity of breast cancer-related arm swelling. Psychological morbidity of lymphoedema. Cancer 1993; 72:3248–52.[CrossRef][Medline]
  14. Sener SF, Winchester DJ, Martz CH, et al. Lymphedema after sentinel lymphadenectomy for breast carcinoma. Cancer 2001; 92(4):748–52.[CrossRef][Medline]
  15. Wilke LG, McCall LM, Posther KE, et al. Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 2006; 13(4):491–500.[Abstract/Free Full Text]
  16. Layeeque R, Kepple J, Henry-Tillman RS, Adkins L, Kass R, Colvert M, Gibson R, Mancino A, Korourian S, Klimberg VS. Intraoperative subareolar radioisotope injection for immediate sentinel lymph node biopsy. Ann Surg 2004; 239(6):841–5; discussion 845–8.[CrossRef][Medline]
  17. Descriptive Statistics. www.physics.csbsju.edu/stats/cstatsNROW_form.Html.
  18. Fisher B, Slack NH. Number of lymph nodes examined and the prognosis of breast carcinoma. Surg Gynecol Obstet 1970; 131:79.[Medline]
  19. Fisher B, Fisher ER, Redmond C. Ten-year results from the National Surgical Adjuvant Breast and Bowel Project (NSABP) clinical trial evaluating the use of Lphenylalanine mustard (L-PAM) in the management of primary breast cancer. J Clin Oncol 1986; 4:929.[Abstract/Free Full Text]
  20. Giuliano A, Schwartz G. Summary of the proceedings of the Philadelphia Consensus conference on the role of sentinel lymph node biopsy in carcinoma of the breast. Semin Breast Dis 2002; 5:110.
  21. Noguchi M, Taniya T, Ohta N, et al. Lymph node metastases versus DNA ploidy as prognostic factors for invasive ductal carcinoma of the breast. Breast Cancer Res Treat 1991; 19(1):23–31.[CrossRef][Medline]
  22. http://www.cancer.org/downloads/STT/CA2006fPWsecured.pdf.
  23. http://www.seer.cancer.gov/faststats/sites.php?site=Breast%20Cancer&stat=Incidence.
  24. Bland K, Copeland E. The Breast: Comprehensive Management of Benign and Malignant Disorders 3rd ed. Saunders: St. Louis; 2004.
  25. Kissin MW, della Rovere QG, Easton D, Westbury G. Risk of lymphedema following the treatment of breast cancer. Br J Surg 1986; 73:580–4.[Medline]
  26. Delouche G, Bachelot F, Premont M, Kurtz JM. Conservation treatment of early breast cancer: long term results and complications. Int J Radiat Oncol Biol Phys 1987; 13:29–34.[Medline]
  27. Larson D, Weinstein M, Goldberg I, et al. Edema of the arm as a function of the extent of axillary surgery in patients with stage I-II carcinoma of the breast treated with primary radiotherapy. Int J Radiat Oncol Biol Phys 1986; 12:1575–82.[Medline]
  28. Petrek JA, Senie RT, Peters M, et al. Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 2001; 92:1368–77.[CrossRef][Medline]
  29. Velanovich V, Szymanski W. Quality of life of breast cancer patients with lymphedema. Am J Surg 1999; 177:184–7.[CrossRef][Medline]
  30. Kwan W, Jackson J, Weir LM, et al. Chronic arm morbidity after curative breast cancer treatment: prevalence and impact on quality of life. J Clin Oncol 2002; 20:4242–8.[Abstract/Free Full Text]
  31. Silberman AW, McVay C, Cohen JS, et al. Comparative morbidity of axillary lymph node dissection and the sentinel lymph node technique: implications for patients with breast cancer. Ann Surg 2004; 240:1–6.[CrossRef][Medline]
  32. Sener SF, Winchester DJ, Martz CH, et al. Lymphedema after sentinel lymphadenectomy for breast carcinoma. Cancer 2001; 92:748––52.[CrossRef][Medline]
  33. Britton TM, Buczacki SJ, Turner CL, et al. Venous changes and lymphedema 4 years after axillary surgery for breast cancer. Br J Surg 2007; Epub Mar 2007.
  34. Soran A, D’Angelo G, Begovic M, et al. Breast cancer-related lymphedema—what are the significant predictors and how they affect the severity of lymphedema. Breast J 2006; 12(6):536–43.[CrossRef][Medline]
  35. McMasters KM, Giuliano AE, Ross MI, Reintgen DS, Hunt KK, Byrd DR, Klimberg VS, Whitworth PW, Tafra LC, Edwards MJ. Sentinel Lymph Node Biopsy for Breast Cancer—Not Yet the Standard of Care. N Engl J Med. 1998; 339:990–995.[Free Full Text]
  36. Leidenius M, Leppanen E, Krogerus L, et al. Motion restriction and axillary web syndrome after sentinel node biopsy and axillary clearance in breast cancer. Am J Surg 2003; 185:127–30.[CrossRef][Medline]
  37. Burak WE, Hollenbeck ST, Zervos EE, et al. Sentinel lymph node biopsy results in less post operative morbidity compared with axillary lymph node dissection for breast cancer. Am J Surg 2002; 183:23–7.[CrossRef][Medline]
  38. Rubio IT, Korourian S, Colvert M, Westbrook KC, Klimberg VS. Sentinel Lymph Node Biopsy for the Staging of Breast Cancer. Am J Surg 1998; 176(6):532–7.[CrossRef][Medline]
  39. Sakorafas GH, Peros G, Cataliotti L, et al. Lymphedema following axillary lymph node dissection for breast cancer. Surg Oncol 2006; 15(3):153–65.[CrossRef][Medline]
  40. Uren RF, Howman-Giles R, Thompson JF. Patterns of lymphatic drainage from the skin in patients with melanoma. J Nucl Med 2003; 44(4):570–82.[Abstract/Free Full Text]



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