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 Table of Contents  
Year : 2022  |  Volume : 42  |  Issue : 2  |  Page : 64-71

The Dual Method (Dye and Ultrasound) for Axillary Mapping in Patients Receiving Neoadjuvant Chemotherapy for Locally Advanced Breast Cancer

1 Department of General Surgery, VMMC and Safdarjung Hospital, Delhi, India
2 Department of Obstetrics and Gynaecology, VMMC and Safdarjung Hospital, Delhi, India

Date of Submission14-Dec-2020
Date of Decision05-Mar-2021
Date of Acceptance09-Apr-2021
Date of Web Publication30-Oct-2021

Correspondence Address:
Dr Deepak Kumar
Room No. 18, Residents' Doctors' Hostel, VMMC and Safdarjung Hospital, Delhi - 110 029
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmedsci.jmedsci_416_20

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Background: Sentinel lymph node (SLN) remains one of the most important indicators of axillary lymph node status, defining the prognosis of breast cancer (BC) patients. The present study was done to map axillary SLN using dual method of intraoperative axillary ultrasound-guided (USG) and methylene blue dye, in patients receiving neoadjuvant chemotherapy (NAT) for locally advanced BC. Methods: A prospective interventional cross-sectional study was conducted on 36 core-needle biopsy-proven cases of locally advanced breast carcinoma (Stage IIb and Stage III) who received NAT. The SLNs as identified by the bluest staining node (dye method) and the node with a needle inserted in it through axillary USG method were dissected and sent for frozen section in normal saline. It was followed by complete axillary dissection and final histopathology reporting. Diagnostic test was used for calculation of sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV). Results: After NAT, 26/29 patients with pre-NAT staging of N1 and 5/7 patients with pre-NAT staging of N2 showed significant downstaging of the nodal status after NAT (P < 0.001). We found that the dual method showed similar sensitivity to the dye method and the USG method (94.74%). But, the specificity, PPV, and NPV of the dual method although similar to the dye method (76.47%, 81.82%, and 92.86%, respectively) were lower than that of the USG method (82.35%, 85.71%, and 93.33%, respectively). Conclusion: In conclusion, dual method (dye and USG) is a good attempt in increasing the SLN detection but it is not a powerful test in the application of avoiding axillary lymph node dissection. The comparable sensitivity but lower specificity in determining the SLN restricts its use, and warrants future studies with contrast-enhanced USG to decrease the false negatives.

Keywords: Dual method, methylene blue dye, sentinel lymph node, ultrasound

How to cite this article:
Kumar D, Chintamani, Naghma S, Gupta S. The Dual Method (Dye and Ultrasound) for Axillary Mapping in Patients Receiving Neoadjuvant Chemotherapy for Locally Advanced Breast Cancer. J Med Sci 2022;42:64-71

How to cite this URL:
Kumar D, Chintamani, Naghma S, Gupta S. The Dual Method (Dye and Ultrasound) for Axillary Mapping in Patients Receiving Neoadjuvant Chemotherapy for Locally Advanced Breast Cancer. J Med Sci [serial online] 2022 [cited 2022 May 27];42:64-71. Available from: https://www.jmedscindmc.com/text.asp?2022/42/2/64/329726

  Introduction Top

Sentinel lymph node (SLN), the first drainage lymph node basin, remains one of the most important indicators of the axillary lymph node status – defining the prognosis of breast cancer (BC) patients.[1] In India, BC ranks number one cancer among females with age-adjusted rate as high as 25.8/100,000 women with a mortality of 12.7/100,000 women.[2]

Locally advanced BC (LABC) is an important subset of BC portrayed by advanced local spread in the absence of distant metastasis. It carries a dismal prognosis due to high association rate of locoregional and systemic failure despite the best of the surgeries. A multimodal approach (surgery, chemotherapy, and radiotherapy in combination with hormonal and targeted therapy if required) is deemed necessary to improve the outcomes.[3] The use of neoadjuvant chemotherapy (NAT) in such cases has shown variable improvement in the outcomes but is certainly reasonable in inoperable cases to increase the odds of R0 resection.[4]

NAT is an effective treatment for downstaging the disease and determining the chemosensitivity of BC.[5] Literature reports tumor downstaging in around 94% of the cases with pathological complete response in 20%–40% of patients after NAT.[6],[7],[8],[9],[10] Evidence also indicates its effect on nodal staging. Krag et al.[11] reports that NAT can clear axillary metastases in 23% cases of LABC which may increase to 40%–60% with simultaneous anti-Her2 therapies.[12]

Since there is no complete cure of the nodal status post NAT, the standard treatment of the axilla after NAT has been an axillary lymph node dissection (ALND).[13] However, because of the side effects which include lymphedema, pain, stiffness, and shoulder weakness and based on the recent results of the Z0011 study, ALND has lost its importance and it seems that the intraoperative explanation of the SLN status is not as obligatory as before.[14],[15],[16],[17],[18]

In certain cases with unfavorable prognosis such as those with LABC, axillary mapping post NAT is very important because it helps specialists for best management.[19] SLN biopsy is an ideal nodal staging method for BC which is equivalent to ALND if performed properly.[8],[20],[21] The traditional methods of the use of methylene blue dye carry a high sensitivity of 93%[22] and 82% (if combined with radioisotope with gamma probe detection);[11] but produce high false-negative results. On the other hand, axillary ultrasound-guided (USG) which has also been used by few investigators for axillary mapping, carries a low sensitivity of 56%–73% but high specificity of 70%–100%.[23],[24],[25] It would thus be of great surgical concern to assess the diagnostic accuracy of a combination of methods – one with high sensitivity and the other with high specificity, to be proficient to detect SLNs.

The current study was conducted to map axillary SLN using the dual method (intraoperative axillary USG and methylene blue dye) in patients receiving NAT for LABC.

  Materials and Methods Top

The proposed prospective interventional cross-sectional study was conducted in the Department of Surgery, Pathology, and Radiology, at a tertiary care hospital, New Delhi, for a period of 18 months (October 2015 to March 2017). The study was approved by the Institutional Ethical Committee (IEC/VMMC/SJH/Thesis/October 2015/29).

Material/patient recruitment

After obtaining informed consent from patients, we recruited 36 core-needle biopsy-confirmed cases of locally advanced breast carcinoma (LABC, Stage IIb, and Stage III) who received NAT. Patients without clinically palpable lymph nodes, frank metastasis, and those not willing to take NAT were excluded from the study.

The sample size calculation was based on the study of Omranipour et al.[19] who observed that the sensitivity and specificity of dye method for predicting axillary lymph node metastasis was 89.5% and 96.6%, respectively. Taking these values as a reference, the minimum required sample size with a desired precision of 20%, 90% power of study, and 5% level of significance was 36 patients. So, the total sample size taken was 36.

All patients were subjected to triple assessment, that is, through clinical examination, imaging (mammography, USG, and magnetic resonance imaging only in equivocal cases), and biopsy for accurate measurement of the basal tumor size and in order to stage the disease accurately. The 8th edition of AJCC (2017) was used for the final staging.[15],[16],[17],[18]

These patients were then subjected to blood investigations including complete hemogram, liver function tests, kidney function tests and serum electrolytes, and echocardiogram before initiation of NAT that were administered in standard doses at three-weekly intervals (cyclophosphamide 500 mg/m2, adriamycin 50 mg/m2 [methotrexate in cardiac patients] and 5-FU 500 mg/m2). All cases were re-assessed clinically and with ultrasonography of the breast (using RECIST, i.e., Response Evaluation Criteria in Solid Tumors) for response assessment after each cycle. Responders were defined as those patients where the tumor size reduced by more than 50% and the axilla was down staged to N0. After the completion of three cycles of NAT (CAF regime), the patients were taken up for surgery.

Sentinel lymph node detection and dissection method

For the current study, the detection of SLN was carried out in steps to compare the individual procedures (dye and US) and dual method using both dye and US.

For the dye method, 3 mL of 1% methylene blue dye was injected intradermally in circumareolar region [Figure 1] followed by 5 min of breast massage to facilitate lymphatic drainage into the lymph node basin.[1]
Figure 1: The periareolar injection of methylene blue dye

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Simultaneously, axillary US (AUS) was performed using a 10-MHz linear array transducer [Figure 2]. Careful examination in the axillary basin was performed using the AUS technique where the sentinel node was identified by tracing along the line of tumor toward the axilla.[5],[26],[27] The identification of the involved node was based on the size and echo pattern and a needle was put on the suspected node on US [Figure 3].[28]
Figure 2: A procedure of intraoperative axillary ultrasound

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Figure 3: A case of ultrasound-guided needle placement in the sentinel lymph node

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An incision was made extending medial to the border of the pectoralis major muscle. Axillary dissection was used to identify the dye-filled lymphatic channel which was then followed distally until a blue-stained node is seen [Figure 4]. The sentinel nodes as identified by the bluest staining node (dye method) and the node with a needle inserted in it (US method) were dissected and sent for frozen section (FS) in normal saline. If the blue node and the node with the needle inserted into it was same [Figure 5]a and [Figure 5]b, then only a single node was dissected and sent for FS.
Figure 4: A dissected blue sentinel lymph node

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Figure 5: The ultrasound -guided needle that pierced through the blue sentinel lymph node. (a) USG guided needle piercing through the blue node. (b) Dissected node showing pierced needle

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Thereafter, MRM with complete ALND of levels – I, II, III – nodes was completed and the specimen was sent in a separate container in formalin for final histopathology. The complete procedural study design is shown in [Figure 6].
Figure 6: Procedural study design

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These were studied for confirmation of diagnosis and accurate tumor size, confirmation of nodal status (pTNM), histological grading, final histopathological margin assessment with a special emphasis on the distance of the tumor from the resected margins, presence of carcinoma in situ in the margins, antigen expression profile and any change in the profile of ER/PR/HER-2-neu, and metastasis to serve as gold standard against which the sensitivity/specificity and accuracy of sentinel node biopsy were calculated.


Categorical variables were presented in number and percentage (%) and continuous variables were presented as mean ± standard deviation (SD) and median. Qualitative variables were associated using the Chi-Square test. Diagnostic test was used for the calculation of sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV). A P < 0.05 was considered statistically significant. The data were entered in MS EXCEL spreadsheet and analysis was done using Statistical Package for the Social Sciences, IBM manufacturer, Chicago, USA, version 21.0.

  Results Top

The final analysis was conducted on 36 patients.

Result 1: Demography and clinical characteristics

The mean age (±SD) was 48.22 (±7.4) years. Half (50%) of the tumors were present on the left side; 66.67% of the tumors were in the T3 stage, followed by 30.56% in the T2 stage and 1 (2.78%) in the T4b stage. 80.56% of the tumors were in the N1 stage and the remaining (19.44%) in the N2 stage. The number of premenopausal and postmenopausal women was 52.78% and 47.22%, respectively. Past history of hypertension and hypothyroidism was present in 2 (5.56%) and 1 (2.78%) patient, respectively. MRM was performed in 97.22% of the patients and BCS in 1 (2.78%) patient. ER, PR, and Her2-neu were positive in 50.00%, 44.44%, and 27.78% patients, respectively. The majority (66.67%) of screening mammograms before surgery fell into BIRADS-5, followed by BIRADS-4 in 25.00% and BIRADS-6 in 3 (8.33%) patients. The mean (±SD) duration of the tumor was 6.22 (±7.6) months [Table 1].
Table 1: Distribution of demography and clinical characteristics of study subjects

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Result 2: Neoadjuvant chemotherapy and nodal status

After NAT, 26/29 patients with pre-NAT staging of N1 and 5/7 patients with pre-NAT staging of N2 showed significant downstaging of the nodal status after NAT (P < 0.001) [Table 2].
Table 2: Nodal status pre and post neoadjuvant chemotherapy

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Result 3: Diagnostic accuracy of the dye method and USG method for detecting metastasis in axillary lymph nodes

We found that the dual method showed similar sensitivity to the dye method and the USG method (94.74%). But, the specificity, PPV, and NPV of the dual method although similar to the dye method (76.47%, 81.82%, and 92.86%, respectively) were lower than that of the USG method (82.35%, 85.71%, and 93.33%, respectively) [Table 3].
Table 3: Diagnostic accuracy of the dye, ultrasound, and the dual methods

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  Discussion Top

The dual method (dye and USG) was applied in the study to know if it could improve the axillary SLN determination. The study was in direct comparison to one of the studies by Li et al. on 453 patients with early invasive BC.[29] The difference is that their study used preoperative contrast-enhanced USG (CEUS) and matched it with intraoperative SLN biopsy using gentian violet dye, whereas our study used intraoperative US with needle marking of the SLN and matched it with methylene blue dye-based SLNB through FS.

The sensitivity, specificity, PPV, and NPV of the dual method in the index study were 94.74%, 76.47%, 81.82%, and 92.86%, respectively, which was comparatively less than that of combined SLN-CEUS (96.82%, 91.91%, 87.54%, and 98.01%, respectively) in the study by Li et al.[29]

The present study showed that the dye method may help mark blue color to the SLN and the USG guidance may help mark the SLN with the needle, both of which can be seen during the axillary dissection, but considering the fact that the dual method showed no improvement in the diagnostic accuracy for SLN, its use in the current practice to spare ALND remains an enigma.

The results of the present study elucidated that USG alone was the most accurate method in detecting axillary metastasis as compared to the dye method and dual method. The study results provide a conclusive answer to the query raised by Jozsa et al. that if radiological information could be combined with salient clinical and histopathological findings, it may enable clinching more cases of nodal involvement.[30] It is to be highlighted that the data support a move toward skipping SNB in patients with a radiologically normal axilla, in the context of high specificity of USG as noted in cases of LABC post-NAT.

The dual method showed good sensitivity of 94.74% which was similar to that of the dye method and USG alone but it fell short for being used in practice due to its high false negatives as the specificity was only 76.47%. Interesting to note was the high sensitivity of USG alone (94.74%) as compared to that of some previous studies which reported a lower range of USG sensitivity.[23],[24],[25] The higher sensitivity might be because we included biopsy-confirmed cases of BC with full details of their pre-NAT nodal staging.

Concurrent with these high false negatives in the present study might be the shortcoming of the dye method alone. Even a latest meta-analysis of 18 studies found a high Sn of 91% with a false-negative rate of 13% for the dye method.[31] The mapping of SLN locations thus seems unacceptable with the dye method alone as is also recommended by the American Society of Breast Surgeons'.

In view of these various trials that have been continuing to adjudicate the dye method with other simultaneous methods, the current study holds strength in providing the relevant data of one of the techniques of SLN detection. Among other researchers, Zhao et al. considered CEUS as a feasible approach for SLN identification with a sensitivity, specificity, PPV, NPV, and accuracy of predicting SLN metastases as 100%, 52.0%, 43.4%, 100%, and 64.9%, respectively.[32] In Garcia-Uribe et al.'s study, the dual-modality photoacoustic and ultrasonic imaging system was used to noninvasively detect SLNs based on the accumulation of methylene blue dye which showed significant results. Intra-nodal pressure (INP) measurement as a new, simple, and quick test (introduced by Nathanson and Mahan Nathanson et al.[33],[34]) was improvised by Omranipour et al.[19] who found significant differences between INP in normal and metastatic lymph nodes. They showed that a combination of INP and level of suspicion (LOS) increased the specificity to 91.7% as compared to INP alone (87%) and USG alone (75.5%).

Results by Omranipour et al.[19] also found the differences in INP based on Her2 neu positivity. This has been explored in one of more of the studies where age, tumor size, LVI, and molecular subtype were taken as statistically significant factors for predicting the risk of LN metastases.[35] Based on that, a risk factor model was also proposed for nodal involvement. Ding et al. also demonstrated that age, tumor size, and histological grade were three independent predictive factors for SLN metastasis in early BC patients.[36] These reports point out that besides clinical, radiological, and histopathological findings, other associated prognostic parameters also help in increasing the predictive accuracy for nodal involvement.

In practice, FS analysis is the most frequently used practice in the assessment of SLN status intraoperatively. However, this method is expensive, needs an expert pathologist reporting, and is associated with false-negative results, tissue loss, and therefore is accused of missing micrometastatic disease.[37] Although the dual method here does not replace the need for FS of the SLN, its use needs further exploration on the basis of molecular subtypes and post-NAT nodal status.

In our study, among those who were missed on the dual method, there were equivalent cases of nodal positive and nodal negative and thus we could not associate the false negatives with post-NAT nodal status. We could not determine an association with the changes that the NAT could cause in the nodes which may lead to false negatives by dye method or USG methods. However, the LOS may be kept if the dual method picks the same node of axillary basin for SLN biopsy.

The use of preoperative NAT and SLN biopsy and knowing the intraoperative nodal status have been an attempt to spare ALND in BC patients. Laws et al. demonstrated the feasibility of minimizing axillary surgery in N1 patients treated with NAC with the use of SLNB.[38] However, they also pointed out some important technical limitations of high false-negative rates for intraoperative SLN evaluation, particularly for patients with small residual nodal volumes.

The study results hold future implication as it suggests that even the combination of investigations may not increase the detection of SLN to avoid ALND. Theoretically, it may sound feasible and good option of using two investigative modalities to have a better diagnostic accuracy, but this was negated in the present study.

Limitations of the study

However, the findings of the study must be interpreted under certain limitations such as small sample size and being conducted at a single center. Second, the effects of NAT on the nodal architecture and micrometastasis was not assessed, though that was not the objective of the study.

Third, the method of taking SLNB post-NAT was not focused as it may have an effect on the diagnostic accuracy.[39]

Lastly, the specificity of the combined assessment remained low, indicating further research on larger sample size and the use of contrast-enhanced US.

  Conclusion Top

In conclusion, the dual method (dye and USG) is a good attempt in increasing the SLN detection but it is not a powerful test in the application of avoiding ALND. The comparable sensitivity but lower specificity in determining the SLN restricts its use, and warrants future studies with CEUS to decrease the false negatives.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]

  [Table 1], [Table 2], [Table 3]


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