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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:438-443 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Sentinel Lymph Node Detection for Breast Cancer: Which Patients Are Best Suited for the Patent Blue Dye Only Method of Identification?

Claude Nos, MD, Paul Fréneaux, MD, Sandrine Guilbert, MD, Marie C. Falcou, DM, Remi J. Salmon, MD and Krishna B. Clough, MD

From the Departments of Surgery (CN, SG, RJS, KBC), Pathology (PF), and Biostatistics (MCF), Institut Curie, Paris, France.

Correspondence: Address correspondence and reprint requests to: Dr Claude Nos, Department of Surgery, Institut Curie, 26 Rue d’Ulm, 75005 Paris, France; Fax: 33-144324006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: The objectives of this study were, first, to define the preoperative criteria for using solely the blue dye method and, second, to decrease its operator dependence in predicting axillary lymph node status.

Methods: Two hundred fifty-three women consecutively identified with operable breast cancer underwent sentinel lymph node (SLN) detection by the patent blue dye method followed by completion axillary lymph node dissection. A standard pathological examination was performed for all SLN. Then, a pathological color quality assessment (PCQA), which checked for the presence of the blue dye, was performed on the paraffin blocks of the nonmetastatic SLN. Six preoperative identifiable variables likely to influence the detection rate were examined.

Results: The surgical detection (sd) rate was 84% (213 of 253) and the PCQA rate was 73% (185 of 253). Only breast size (sd, P = .0005; PCQA, P = .0007) and body mass index <=30 (sd, P = .005; PCQA, P = .0007) were significant for SLN identification. Multivariate analysis revealed two independent factors influencing SLN identification: breast size (sd, P = .0001; PCQA, P = .002) and the timing of injection—injection prior to lumpectomy (sd, P =.04).

Conclusions: The optimal patient features for identifying the SLN by the patent blue dye method are small or medium-sized breasts, low body fat, and that the procedure is carried out prior to tumor excision. The PCQA offers a useful second assessment of the surgically removed SLN, introducing an independent element of quality control.

Key Words: Sentinel lymph node biopsy • Breast carcinoma • Axillary dissection • Pathological color quality assessment


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Sentinel lymph node (SLN) biopsy is a fast-developing technique, which offers an alternative to axillary dissection for some breast cancer patients. However, the identification rate for SLN biopsy differs from one medical team to another and also between different techniques.1 There are two techniques available for SLN identification: the isotope method and the patent blue dye method, which may be used individually or in combination. Identification rates reported with the blue dye method range from 70% to 93%, depending upon the surgeon’s experience.1–9 The use of the isotope method has increased the identification rate to over 90%.10–19 It is therefore advocated by many authors—either alone10–13 or in combination with the patent blue dye method.14–19 However, the patent blue dye method is simpler, quicker, and cheaper. Thus, some authors still advocate it as the standard technique1 despite the lower identification rate when the isotope method is omitted. Others argue that SLN identification, using only the patent blue dye method, is unreliable because it is more operator-dependent and leads to poorer identification.1 In practice, many surgeons use only the patent blue dye method to identify the SLN because the isotope technique is more difficult to employ routinely and is more expensive. The objectives of this study were first, to attempt to identify a subgroup of patients for whom the blue dye only method yielded satisfactory results, and second, to explore the role of a second SLN color assessment by the pathologist. We have called this assessment the pathological color quality assessment (PCQA), which introduces an element of quality control with a view to reducing operator dependence with the technique.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
From December 1997 to August 1999, 253 women with invasive, clinically determined T0–2 N0 breast cancer were enrolled in a prospective study of SLN biopsy at the Institut Curie (Paris). All procedures were performed by the patent blue dye method (Bleu patenté V Guerbet, Laboratoire Guerbet, Villepinte, France). All SLN biopsies were followed by a completion axillary lymph node dissection, including level I and II nodes. Seven surgeons participated in the study.

Six variables which might influence the SLN identification were tested: surgeon’s experience, patient’s age, body mass index (BMI), timing of injection in relation to tumor excision, tumor location, and breast size.

Surgeon’s experience:
The first 10 cases performed by each surgeon (one surgeon only performed 8 cases) were identified separately (Table 1). This group of 68 cases was then compared with the remaining 185 patients (Table 2).


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  		TABLE 1. Individual results of sentinel lymph node biopsy by the patent blue dye technique
 

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  		TABLE 2. Univariate analysis of six preoperative criteria (N = 253)
 
Age:
Patients were divided into two age groups: <=50 years (62 patients) and >50 years (191 patients).

Body mass index (BMI):
This was calculated using the Quetelet index: weight (Kg)/height2 (M). BMI information was available on only 234 patients. Twenty-five patients with a BMI >30 made up the obese group and 209 patients with a BMI <=30 made up the nonobese group.

Timing of injection in relation to tumor excision:
All patients were injected with 2 to 5 ml of patent blue dye. The injection was performed intraglandularly and subcutaneously but not intradermally. Breast massage was performed systematically. The injection was peritumoral and before lumpectomy or mastectomy in 165 patients for whom malignancy had been confirmed by fine needle aspiration cytology or core needle biopsy. In 88 patients, the blue dye injection was performed around a biopsy cavity. This was either after frozen section had been used to confirm the malignant nature of the lesion (49 patients) or when an excisional biopsy had been performed as a previous operation (39 patients).

Tumor location:
This was located in the medial (57 patients) or lateral (196 patients) hemisphere of the breast. The hemispheres were defined by using a vertical line passing through the medial border of the areola. Central or subareolar lesions (25 patients) were considered to be in the lateral hemisphere.

Breast size:
Breast size information was available on only 237 patients. Patients were divided into two groups according to bra cup size: cup size D-E (73 patients had large breasts) and cup size A-B-C (164 patients had small or average breasts).

The SLN identified by the surgeon determined the surgical detection rate (i.e., whether one or more SLN were identified for a given patient). The SLN biopsy and completion axillary lymph node dissection were sent to the pathologists. No frozen section was performed on the SLN biopsy. The SLN biopsy and all axillary lymph nodes were bisected and fixed in AFA (alcohol, formalin, and acetic acid) in the following proportions: 5% of 100%-acetic acid, 75% pure ethyl alcohol, 18% demineralized water, and 2% of 40%-formalin. Then they were embedded in paraffin individually. One level of hematoxylin- and eosin-stained slide from each node was examined for the presence of metastatic disease. Then, the nonmetastatic SLN underwent a pathological color quality assessment (PCQA) for the presence of dye. The pathologist performed this by checking the paraffin blocks macroscopically and assessing whether at least one SLN identified by the surgeon was blue or not for any given patient.20

The PCQA rate was then defined as the sum of the nonmetastatic SLNs which were blue stained (as confirmed by the pathologist) and the total number of metastatic SLNs. This was then divided by the total number of patients to determine the PCQA rate, which was expressed as a percentage.

PCQA rate = PCQA positive nonmetastatic SLN + metastatic SLN/total number of patients.

The surgical detection rate and PCQA rate were examined in relation to the different variables previously identified. A multivariate analysis was then performed, using the logistic regression model.21 A forward stepwise procedure was used to select the variables entered in the model. Odds ratios [OR] are presented with their 95% confidence interval [CI].


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
The patients’ mean age was 58 years (range 28–87). Twenty-eight patients (11%) had clinically determined stage T0 tumors, 129 (51%) had T1 tumors, and 96 (38%) had T2 tumors. The surgery performed was either a lumpectomy (229 patients, 90%) or a mastectomy (24 patients, 10%). Mean histological invasive tumor size was 16 mm (range 3–50 mm). The invasive tumors were subclassified as ductal (197 patients, 78%), lobular (42 patients, 17%), or others (13 patients, 5%). Tumor grade was I for 108 patients (43%), II for 107 patients (43%), III for 27 patients (10%), or undetermined for 11 patients (4%). The majority of tumors were estrogen receptor positive (79%) and progesterone receptor positive (65%). The mean number of SLN was 2.0 (range 1–6) and mean number of non-SLN was 11 (range 5–31).

The surgical detection rate of SLN was 84.2% (213 of 253). After standard pathological examination, 61 SLN were found to be metastatic (29%, 61 of 253), 152 SLN were free of disease (71%, 152 of 253), of which 6 SLN were false negatives. The false negative rate was thus 9% (6 of 67). The negative predictive value was 96%. Half the false negative cases arose during the first 10 cases for each surgeon (Table 1). All the false negative cases occurred for tumors located in the lateral hemisphere. One false negative occurred in a patient after prior excisional biopsy.

Univariate analysis found the two factors that influenced the detection of SLN to be breast size and BMI. Patients with small or normal-sized breasts had a better surgical detection rate than patients with large breasts (P = .0005). Nonobese patients had a better surgical detection rate than patients in the obese group (P = .005). Other factors were not significant (Table 2). Multivariate analysis found that two factors remained significant for SLN surgical detection: (a) breast size (P = .0001) and (b) timing of injection in relation to tumor excision—injection prior to surgery compared to injection after lumpectomy (P = .04) (Table 3).


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  		TABLE 3. Surgical detection rate: Results of multivariate analysis
 
The PCQA rate was 73.1% (185 of 253). One hundred twenty-four of 152 negative sentinel nodes were blue stained. Three of six false negative sentinel nodes were not blue stained (PCQA negative) (Table 1). Univariate analysis found the factors that influenced the PCQA detection of the SLN to be: (a) breast size: small or normal-sized breasts compared to large breasts (P = .0007), (b) BMI: nonobese patients compared to obese patients (P = .0007) and, (c) timing of injection—injection prior to surgery of patent blue dye compared to injection after lumpectomy (P = .04). Other factors were not significant (Table 2). Multivariate analysis determined that the only independent factor influencing the PCQA detection was breast size: small or normal-sized breasts compared with large breasts (P = .0001). Age and timing of injection in relation to tumor excision both impacted on the PCQA but were statistically dependent (Table 4). Thus, patients less than 50 years old, for whom a blue dye injection was performed prior to surgery, had a significantly higher PCQA rate (OR = 8) than if the injection was performed after tumor removal. For patients greater than 50 years old, the PCQA was identical regardless of the timing of injection.


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  		TABLE 4. Pathological color quality assessment: Results of multivariate analysis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
This study demonstrates that, after a multivariate analysis of clinical factors, only three factors predict SLN detection with patent blue dye: breast size, BMI, and timing of injection with respect to tumor excision. This was defined in terms of correctly predicting axillary node status. In our series, we used a routine control of the coloration of the excised SLN by the pathologist (PCQA) because blue dye SLN technique is operator dependent and clinical factors that influence lymphatic mapping are difficult to establish. A postoperative check of the color of the SLN biopsy is a simple method which introduces the notion of quality control for the SLN specimen. This pathological verification is intended to double-check the technique by enabling a retrospective confirmation that the specimen was a true SLN biopsy.20 This quality assessment is particularly important with negative SLNs, because it forces the surgeon to remove a true blue-stained SLN and differentiates SLN biopsy from a blind lymph node sampling. PCQA is unnecessary for histologically proven metastatic SLN because false positive results do not occur by definition. Furthermore, SLN which are extensively replaced by tumor may be nonfunctional, block the lymphatic flow of dye, and may not be stained blue.6,15 The aim of the quality assessment (PCQA) of the SLN was to decrease the operator-dependent nature of the technique by introducing a double-check that the surgically excised SLN was blue.

We used the peritumoral injection method which is the most widely reported in the literature.2–7,9,10,12–19

The SLN was detected by following the blue lymphatic pathway(s) to its first node in the axilla. So, in principle, the tumor, the lymphatic vessel, and the SLN should be stained blue because there is a continuum of the metastatic lymphatic diffusion.

The determining factors for the successful application of the blue dye method alone in identifying sentinel lymph nodes are not clearly established. In our series, we used the surgical detection rate, PCQA rate, and the false negative rate to determine which patients would obtain a satisfactory result from the use of the blue dye method and would not require radioactive colloid detection. This was defined in terms of correctly predicting the axillary status. It is generally agreed that approximately 30 cases of SLN biopsy and completion axillary lymph node dissection are required for a surgeon to become proficient in the SLN technique, and the surgeon’s experience is the best known predictive factor for obtaining a reliable result.15 In our series, surprisingly, surgical experience was not a determining factor in identifying the SLN. This held true for both the surgical detection rate and the PCQA rate. We considered that the first 10 cases would constitute the surgeon’s learning curve, taking into account that all seven surgeons worked closely as a team and could benefit from each others’ experience.3,17 However 3 of 6 false negative results occurred during the surgeons’ first 10 cases (Table 1). In this series, the learning period did not appear to influence the identification of the sentinel node, but it is important for minimizing the false negative rate.

Univariate analysis of the surgical detection rate and PCQA identification rate shows that the predictive factors for identification of the SLN by blue dye are the same: namely, breast size and BMI. A multivariate analysis of surgical detection rate and PCQA identification rate shows that breast size is the most significant factor in identifying the SLN.

Interpretation of breast size is, however, subjective and has rarely been analyzed in other articles. The identification rate is almost certainly linked to the size of the axilla. The search for blue-stained lymphatic vessels and blue SLN is more difficult in a voluminous and adipose axilla than if the patient is thin. The body mass index is an independent factor in this study. In obese patients, the breasts are fatty and the capacity of lymph nodes to retain the blue dye may be decreased because lymph nodes can be replaced by fat in these patients. Age (over 50 years) is also a factor that impacts the identification rate of the sentinel node10 even though it was not found to be statistically significant in this study. Krag10 showed, using the isotope technique alone, that age over 50 was an independent factor in lowering the identification rate of the SLN, possibly due to lymph node fatty replacement. Therefore, it would seem that the search for the SLN in obese patients is more difficult not only by the blue dye method but also by the isotope method. Under these conditions, in order to increase the identification rate for these patients, it is probably necessary to use both the isotope and blue dye techniques. Increasing radioactive tracer doses may also be helpful.10

The second independent factor influencing SLN identification was the timing of injection in relation to the lumpectomy. SLN biopsy should be performed prior to tumor excision. This parameter is significant in surgical identification of the SLN but is linked to age for identification by PCQA. Thus, peritumoral injection is particularly beneficial to young patients because it increases the chances of finding a blue node. Injection in the tumor bed, after excision for frozen section confirmation of malignancy or prior excisional biopsy, leads to significantly lower SLN identification rates.

Opinions in literature differ concerning the identification rate of the SLN—by injection of the dye or radioactive tracer in the tumor bed—after prior excisional biopsy. Some investigators have observed lower identification rate of SLN after prior excisional biopsy when using vital blue dye (as in our study) or radioactive colloid.10,12 Others have had equal success regardless of a prior biopsy, both using vital dye6,7 or combined techniques.16,18 However, these same investigators do not advise using SLN biopsy for patients with extensive previous surgical biopsy (specimen >6 cm),6 especially when located in the upper outer quadrant of the breast.16 In the Memorial Sloan-Kettering16 series, most of the false negative cases occurred when injection was performed into the tumor bed after excisional biopsy.

A prior excisional biopsy therefore constitutes a relative contraindication for the SLN technique that uses a peritumoral injection. Consequently, after analyzing the results of our study, we now recommend the search of the SLN by peritumoral injection after preoperative diagnosis by fine needle aspiration or core needle biopsy. Where tumors have already been removed by large excisional biopsies, alternative methods of injection such as subareolar may prove more reliable, but further studies are required. Lastly, medial location of the tumor decreased, but not significantly, the blue dye identification rate of the SLN in the axilla. This is at least partially due to the physiologic drainage of the breast, because not all the areas of the breast drain towards the axilla.13 The absence of a SLN in the axilla is not necessarily a failure of the technique. It should however, ideally, lead to further inspection for a SLN in other nodal fields (i.e., internal mammary, infra/supra clavicular). This is unfortunately not possible with the blue dye method alone, and it, therefore, justifies isotope mapping with colloid injection using a peritumoral radioactive colloid injection in order to reveal nonaxillary lymph drainage. However, it is noteworthy that the accuracy of the axillary SLN, in terms of false negative rate for medially located tumors, appears good. In our series, no false negative were found for a medially located tumor. This was also the finding of the Memorial Sloan-Kettering16 series and in the multicenter study carried out by Krag et al.10 However, both studies used isotope detection.

Regarding our study, breast carcinoma patients who had a combination of two criteria: small to medium-sized breasts and no excision biopsy of the tumor (113 patients), had a surgical detection rate of 93.5% and PCQA rate of 87%. On the other hand, the 15 patients of this current series with large-sized breasts, and who had undergone tumor excision prior to SLN biopsy, had a surgical detection rate which was only 53% and PCQA rate of 46%.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
In our series, using only the blue dye method to identify the SLN, the best results, in terms of identification of the SLN by the surgeon and confirmation that nonmetastatic SLN were blue (PCQA), were achieved for patients with small to medium-sized breasts, low body fat, and who had not undergone prior tumor excision. In patients with large breasts, who are obese, or who have had a prior excisional biopsy, the results of the SLN technique using blue dye alone are unreliable and this technique can not be recommended for these patients.


   Acknowledgments
 
The authors thank Dr Jeremy Hurren for his valued contribution to this article. Surgeons who took part in the study are: Dr Didier Bourgeois, Dr Jean-Yves Charvolin, Dr Krishna Clough, Dr Jean-Noel Guglielmina, Dr Jean-Pierre Hamelin, Dr Vincent Jacquin de Margerie, and Dr Claude Nos.

Received for publication September 8, 2000. Accepted for publication January 25, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

  1. Cody III HS. SLN mapping in breast cancer. Oncology 1999; 13: 25–43.
  2. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220: 391–401.[Medline]
  3. Giuliano AE, Jones RC, Brennan M, Statman R. Sentinel lymphadenectomy in breast cancer. J Clin Oncol 1997; 15: 2345–50.[Abstract/Free Full Text]
  4. Flett MM, Going JJ, Stanton PD, Cooke TG. Sentinel node localization in patients with breast cancer. Br J Surg 1998; 85: 991–3.[CrossRef][Medline]
  5. Guenther JM, Krishnamoorthy M, Tan LR. Sentinel lymphadenectomy for breast cancer in a community managed care setting. Cancer J Sci Am 1997; 3: 336–40.[Medline]
  6. Guenther JM. Axillary dissection after unsuccessful sentinel lymphadenectomy for breast cancer. Am Surg 1999; 65: 991–4.[Medline]
  7. Haigh PI, Hansen NM, Qi K, Giuliano AE. Biopsy method and excision volume do not affect success rate of subsequent sentinel lymph node dissection in breast cancer. Ann Surg Oncol 2000; 7: 21–7.[Abstract]
  8. Rodier JF, Janser JC. Surgical technical details improving sentinel nodes and breast cancer. Oncology Rep 1997; 281–3.
  9. Nos C, Bourgeois D, Fréneaux P, Zafrani B, Salmon RJ, Clough KB. Individualisation du ganglion sentinelle en cas de cancer du sein. Experience de l’Institut Curie. Bull Cancer 1999; 86: 580–4.[Medline]
  10. Krag DN, Weaver DL, Ashikaga T, et al. The sentinel node in breast cancer. A multicenter validation study. N Engl J Med 1998; 339: 941–6.[Abstract/Free Full Text]
  11. Veronesi U, Paganelli G, Viale G, et al. Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst 1999; 4: 368–73.
  12. Borgstein PJ, Pijpers R, Comans EF, van Diest PJ, Boom RP, Meijer S. Sentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg 1998; 186: 275–83.[CrossRef][Medline]
  13. Uren RF, Howman-Giles RB, Thompson JF, Malouf D, Ramsey-Stewart G, Niesche FW. Mammary lymphoscintigraphy in breast cancer. J Nucl Med 1995; 36: 1775–80.[Abstract/Free Full Text]
  14. Cox CE, Pendas S, Cox JM, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg 1998; 227: 645–53.[CrossRef][Medline]
  15. Bass SS, Cox CE, Reintgen DS. Learning curves and certification for breast cancer lymphatic mapping. Surg Oncol Clin N Am 1999; 8: 497–509.[Medline]
  16. Hill ADK, Tran KN, Akhurst T, et al. Lessons learned from 500 cases of lymphatic mapping for breast cancer. Ann Surg 1999; 4: 528–35.
  17. Cody III HS, Hill ADK, Tran KN, Brennan MF, Borgen PI. Credentialing for breast lymphatic mapping: how many cases are enough? Ann Surg 1999; 5: 723–72.
  18. Barnwell JM, Arredondo MA, Kollmorgen D, et al. Sentinel node biopsy in breast cancer. Ann Surg Oncol 1998; 5: 126–30.[Abstract]
  19. Van de Ent FWC, Kengen RAM, Van der Poll HAG, Hoofwijk AGM. Sentinel node biopsy in 70 unselected patients with breast cancer: increased feasibility by using 10 mCi radiocolloid in combination with a blue dye tracer. Eur J Surg Oncol 1999; 25: 24–9.[CrossRef][Medline]
  20. Fréneaux P, Nos C, Charvolin JY, et al. Détection des ganglions sentinelles axillaires par le Bleu Patenté au cours de la chirurgie des cancers du sein: proposition pour une validation de la qualité des prélèvements chirurgicaux. Ann Pathol 2000; 20: 545–8.(French)[Medline]
  21. Hosmer DW,DW, Lemeshow S. Applied Logistic Regression. New York: John Wiley and Sons, 1980.



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