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Year : 2012  |  Volume : 49  |  Issue : 1  |  Page : 66-73

Role of axillary sampling in the era of sentinel lymph node biopsy: A critical review

Department of Surgical Disciplines, AIIMS, New Delhi, India

Date of Web Publication25-Jul-2012

Correspondence Address:
V Seenu
Department of Surgical Disciplines, AIIMS, New Delhi
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0019-509X.98923

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 » Abstract 

Axillary lymph node dissection is the standard of care for treating and staging axilla in breast cancer. Sentinel lymph node biopsy and axillary sampling have been advocated as an alternative to axillary lymph node dissection with an added benefit of lesser morbidity. Herein, we are reviewing the role of axillary sampling in the present era of sentinel lymph node biopsy in the background of standard axillary dissection.

Keywords: Axillary sampling, axillary dissection, sentinel lymph node

How to cite this article:
Bassi K K, Seenu V, Srivastava A, Al Sharara N. Role of axillary sampling in the era of sentinel lymph node biopsy: A critical review. Indian J Cancer 2012;49:66-73

How to cite this URL:
Bassi K K, Seenu V, Srivastava A, Al Sharara N. Role of axillary sampling in the era of sentinel lymph node biopsy: A critical review. Indian J Cancer [serial online] 2012 [cited 2022 May 29];49:66-73. Available from:

 » Introduction Top

Axillary lymph node status is the most important prognostic factor in patients with breast cancer. [1] Clinical assessment of the axilla is unreliable and imaging techniques though promising are at present not practical. Recently, molecular classification, independent of tumor grade, size and lymphovascular invasion, based on breast cancer biology has been hypothesized to predict the presence of nodal metastases at diagnosis of early breast cancer, which might facilitate treatment decisions regarding the axilla. [2] However, standard surgical care is the resection of the primary tumor (mastectomy or breast-conserving surgery) with axillary lymph node dissection (ALND). There is potentially significant morbidity following conventional or modified ALND. The important and common complications associated with ALND are seroma, wound infection resulting in delayed wound healing, restriction of shoulder movement, intercostobrachial nerve syndrome (paraesthesia of the axilla, shoulder and upper arm), lymph edema predisposing to cellulitis, rarely lymphangio-sarcoma and Stewart-Treves syndrome. [3],[4],[5],[6],[7] Thus in patients who do not have axillary lymph node metastasis there is a need for a procedure which can stage the axilla as accurately as conventional or modified ALND sans the complications associated with it.

The alternatives available to surgically staging the axilla are sentinel lymph node biopsy (SLNB) [8],[9],[10],[11],[12],[13],[14],[15],[16] and axillary sampling (AS). AS entails the removal of a sufficient number of suspicious lymph nodes with the aim of detecting the presence of lymph nodal metastasis. Various AS methods with different nomenclature and dissimilar techniques have been described in the literature, viz. pectoral lymph node biopsy, four-node AS (4NAS), triple node biopsy, five-node sampling, and anatomically guided lower axillary sampling. [17],[18],[19],[20],[21]

Pectoral lymph node biopsy was introduced to identify those patients in whom postoperative radiotherapy could be safely avoided following simple mastectomy. Cant and Forest et al., described this technique in their historic work pictographically. [17],[22],[23] Pectoral lymph node biopsy has been described as removing the nodes which lie at the upper border of the axillary tail of the breast and also dissecting out lymph nodes from the mastectomy specimen by careful palpation of the axillary tail. [17],[22],[23],[25] The Cardiff-St. Mary's trial (1967) [24] was the first one to compare simple mastectomy and pectoral node biopsy with radical mastectomy, followed by a Scottish trial (1971) [18] studying radical radiotherapy to no radiotherapy in node-negative patients based on pectoral node biopsy results (pectoral node-positive patients were given radiotherapy). There has been a steady evolution of the philosophy of AS from 1967 till 1980 when Forrest et al., recommended that a minimum of four nodes are to be retrieved from the axilla by intra-operative palpation for an adequate nodal sample. [26]

Davies et al., performed axillary sampling (axillary tail nodes from simple mastectomy specimen and nodes from the upper border of the axillary tail as described by Forest et al.,) and reported a false negative rate of 14%. [27] Kissen et al., included all the tissue adjacent to the axillary tail below the level of the intercostobrachial nerve in the axillary sample with a false negative rate of 8% and inability to identify nodes in 10% of cases. [28]

Du Toit et al., studied 'Triple node biopsy' in 1288 patients. Triple node biopsy comprises sampling of three nodes; one node from the lower axilla below the lateral border of the pectoralis minor muscle; second from the apex of the axilla, adjacent to the axillary vein, by splitting the muscle fibers between the sternal and clavicular heads of the pectoralis major muscle, and the third node from the internal mammary chain via the second intercostal space. [19] Ahlgren et al., described a five-node biopsy of the axilla, beginning the dissection at the axillary tail of the breast until five lymph nodes had been removed. [20] Thus, AS has different connotation in terms of the boundaries of the dissection and the number of nodes to be removed.

Parmar et al., attempted to precisely define the anatomical boundaries of low AS (LAS) to ensure the reproducibility of the technique (modified Kissen's technique) and sampling of at least four lymph nodes. The boundaries of LAS as defined by them are: posteriorly, lateral border of the latissimus dorsi muscle, anteriorly lateral border of the pectoralis major muscle, superiorly, intercostobrachial nerve, medially, second digitations of the serratus anterior muscle and the base is formed by the subscapularis muscle and the pedicle of the latissimus dorsi muscle. [21]

Another important issue in AS is the exact number of lymph nodes that need to be removed during AS to correctly identify node-positive patients. A retrospective histological analysis by Cserni et al., showed that sampling three to six largest/firmest nodes can adequately represent the status of rest of axilla. The author reviewed slides from 499 pathologically N1/N0 ALND specimens of breast cancer cases. Two hundred and sixty-five ALND specimens were positive for metastasis. The author numbered the nodes in the sequence of size/ metastatic deposit in the lymph nodes. They observed that evaluation of three to six largest/firmest nodes in each patient can detect 93-98% of node-positive axillae. They concluded that sampling of the four to six largest/firmest nodes can be a reliable alternative for the staging of early breast cancer provided that the operating surgeon is able to identify the suspicious nodes intraoperatively. [29]

There have been arguments for and against the AS in the literature. [30],[31] Kissen et al., and Davies et al., concluded against the AS as a staging procedure of the axilla. [18],[19] Mathiesen et al , stated that the probability of finding at least one metastatic node increased continuously up to about 10 removed nodes from axilla and they concluded that in order to minimize the risk of erroneous staging of axilla, about 10 nodes should be removed. [32] Thus when AS is performed, there is a risk of under-staging the axilla and node-positive patients may go unrecognized and untreated. AS has been evaluated in this regard vis-a-vis ALND and SLNB in several studies.

Axillary sampling versus complete axillary clearance

In some centers in the United Kingdom, AS is an established method of examining the axilla. A survey of surgeons (n=271) has revealed that 20.7% of them use AS as an initial management option in node-negative T1 size tumors. [33]

Steele et al., in a study from Edinburgh, randomized 417 patients (T1-T3/N0-1) to mastectomy + 4NAS versus mastectomy + complete ALND. Radical radiotherapy (breast and axilla) was given to patients with positive 4NAS and not to those patients who underwent complete ALND. The authors described the 4NAS as an accurate procedure when compared with ALND. Only in one AS (0.5%), they failed to identify positive nodes. [26]

Ahlgren et al., performed five-node sampling followed by Level I and II ALND in 415 patients (T0-3/N0/M0). Authors reported a sensitivity of 97.3% and a negative predictive value of 98.5% for five-node biopsy. Based on these findings they proposed five-node dissection as an alternative to axillary clearance in early-stage breast cancer. [20] Barthelmes et al., in a retrospective review comprising 312 patients also validated the concept of AS (average sample=eight nodes) in the management of axilla. [34]

Parmar et al., compared LAS with ALND in 355 breast cancer patients (T1-3/N0) with clinically negative axilla with an overall false negative rate of 8.8% (10 of 114 node-positive axilla). They reported a sensitivity rate of 80.7%, negative predictive value of 96% and accuracy of 79% for LAS to identify metastasis. The sensitivity (95% with six-node sampling) and false negative rate (1.5% with six-node sampling) seemed to improve with the number of sampled nodes, however the results were not statistically significant . [21] Based on the findings of this study, they proposed anatomical guided LAS as a low-cost alternative to SLNB in developing countries.

Tanaka et al., in a study (4NAS followed by ALND) of 237 patients (T1-2/N0-1) revealed that 4NAS may be as accurate staging procedure as ALND and reported an overall false negative rate of 6.5% with 4NAS. Interestingly, 4NAS appeared to be inadequate treatment of the axilla when more than two nodes were involved by the tumor. [35] A similar conclusion had been drawn by Noguchi et al. The authors studied (n=243) the diagnostic value of intraoperative AS (frozen section analysis) in patients with operable breast cancer (TIS, T1-3/N0-2). Initially, they performed partial axillary dissection including Level 1 and 2 lymph nodes along with mastectomy or breast-conserving surgery followed by separate removal of Level 3 lymph nodes. In the operating room, they dissected out one to six hard/enlarged axillary nodes (mean of four nodes) from the partial axillary dissection (Level 1 and 2) specimen. Half of each of these sampled nodes was examined by frozen section. The rest of the sampled nodes, residual nodes in the partial axillary dissection and the nodes dissected at Level 3 were sent separately for conventional histopathological examination. Frozen section examination had a diagnostic accuracy of 92%, sensitivity of 77% and specificity of 100%. AS detected the presence of metastases in 65 of 84 (77%) patients with positive axillary lymph nodes. In the patients in whom the axillary involvement was not identified by AS, however, the extent of axillary involvement was limited to Levels 1 and 2, and the authors suggested that partial axillary dissection may be justified in the patients in whom there are no metastases on AS on frozen section. Whereas a complete axillary dissection should be performed for patients in whom axillary involvement is found by this procedure since a significant number of patients with involved nodes (n=23, 23%) were not identified by AS. [36]

As far as morbidity is concerned both AS and ALND have post-procedure long-term problems. Studies have revealed that AS is a less morbid procedure when compared alone (without addition of radiotherapy) with ALND. Chetty et al., reported significant lymphoedema at three-year follow-up in the ALND group when compared with AS. [37] Forest et al., reported arm morbidity and arm edema in the following order (three groups): 4NAS+ RT> ALND>4NAS. [38] Moffat et al., reported arm edema in the order of AS> partial ALND (Level 1 and 2)> complete ALND. [39] Tanguay et al., in a retrospective review of 381 patients, reported the following rate of lymphoedema at five years following surgery: 5% in the AS group against 18% in the ALND group. [40]

Survival, loco-regional recurrence in axillary sampling and axillary lymph node dissection

In two trials from Edinburgh, 4NAS was performed and these patients were then randomized to undergo complete ALND or no further surgery. Forest et al., (n=417,T1-3/N0-1) reported no difference in survival (ALND-62.6 % vs. AS-65 %). At a median follow-up of 11 years, there was only a minor difference in axillary relapse, favoring axillary clearance (3.0% -AS vs. 5.4%-ALND) and a non-significant increase in the rate of loco-regional relapse (chest wall recurrence-21% ALND group vs. 12% in the AS group in patients with node-positive disease). The increased chest wall recurrence in the ALND group was attributed to not irradiating the chest wall in the clearance group. [38] In a second randomized trial (Chetty et al.,) of 466 patients undergoing breast conservation surgery for tumor size ≤ 4 cm, authors compared AS with ALND. Radiotherapy was given to patients with positive nodes after AS. There was no statistically significant difference in axillary recurrence (8 vs. 7), breast recurrence (14 vs. 15), distant recurrence (29 vs. 29) or five-year disease-free survival (82.1% vs. 88.6%) among the complete ALND and AS groups respectively. [37],[41] Hadjiminas et al., (n=114, Stage I and II tumors) opined that selective approach of performing ALND based on AS (intra-operative contact cytology of four node sample), results in adequate staging of axilla without under-treatment of loco-regional disease. After a median follow-up of 20 months there were no loco-regional /distant metastases in the node-negative group. [42]

On the other hand, the impact of complete ALND on long-term overall and disease-free survival is unclear from the literature. NSABP B-04 did not show any survival advantage following complete axillary clearance in clinically negative axilla, [43] although the study has been criticized for not being adequately powered. [44] The Danish Breast Cancer Cooperative Group (DBCG) reporting on 13,851 breast cancer patients who either underwent total mastectomy or breast conservation therapy along with partial axillary dissection reported to the contrary. They categorized patients into two groups based on tumor size, skin/ fascia invasion and lymph node status. High-risk patients (tumor > 5 cm, and/or positive nodes, and or skin/fascia invasion) had received adjuvant systemic therapy and/or radiotherapy. Low-risk patients (tumors up to 5 cm , and negative nodes, and no skin/fascia invasion) were observed and received no adjuvant therapy. In the low-risk group (n =7145), they reported a highly significant correlation between the number of nodes examined and axillary recurrence-free survival, overall recurrence-free survival and overall survival. The study revealed that patients in whom 10 or more lymph nodes were examined and were negative for metastasis had a significantly better axillary recurrence-free survival (P < 0.000l), overall recurrence-free survival (P < 0.0001) and overall survival (P < 0.005) compared with patients in whom less than 10 nodes were removed and examined. [45] Orr et al., in a meta-analysis of six trials spanning four decades and 3000 patients, credited a survival advantage of 5.4% (4-16%) to prophylactic ALND in clinically negative axilla. [46] These findings were corroborated by Krag et al., on analysis of 72102 patients of breast cancer from the Surveillance, Epidemiology and End Results (SEER) database. [47] The EBCTCG meta-analysis (subgroup analysis of four trials) also implied advantage for ALND over no ALND in clinically negative axilla. [48]

However, it is important to note that in all these studies, patients in either group have not received any systemic adjuvant treatment which has proven benefits in terms of long-term survival and loco-regional recurrences. In addition, most of these studies reported on patients treated over a long period of time spanning more than a few decades in some cases, during which time enormous changes have taken place in the adjuvant treatment methods.

Axillary sampling versus sentinel lymph node biopsy

SLNB is a guided, precise and reproducible minimally invasive technique for staging early tumors (T1-2). [49] However, it requires radiocolloid and gamma probe or blue dye. Utility of SLNB in staging clinically node-negative axilla is well-established now. [50] Whereas AS is a relatively blind procedure, not completely non-anatomical.

Is there is an overlap between sentinel nodes and sampled nodes from the axilla? The sentinel lymph node is found mostly at nodal Level 1 medial to the lateral border of the pectoral major muscle and axillary sampling is done from the low axilla after giving a skin incision below the axillary hairline. However germane of the AS is that which four nodes to pick from an axillary basket of 50 nodes? Cserni G. studied 40 patients with palpable T1 and T2 breast carcinoma. They underwent SLNB following mapping with patent blue dye, with subsequent axillary clearance and treatment of primary tumor. All blue nodes were considered SLNs. All the nodes were arranged in order of their size, also consideration w asgiven to lymphoid tissue and metastatic deposits in the node based on staining with H and E. Then the largest/firmest three, four, five and six nodes were selected from all the lymph nodes mimicking an axillary sample thinking that these are the most likely ones to be sampled, because of their size and consistency. The probability of the SLNs falling into the sample of the three to six largest/firmest nodes was calculated. The SLNs predicted the axillary nodal status in 95%, while the samples of the largest three, four, five and six nodes were predictive in 95%, 96%, 98% and 98%, respectively. The SLN would have overlapped with the sample of the three to six largest/firmest nodes in 79-92% of the cases, depending on the number of (largest/firmest) nodes evaluated. [51] But either procedure cannot be done without influencing the other, so the validity of the study is under question. The Breast Unit, Nottingham (Macmillan et al.,) in a study comparing SLNB with AS found that SLN was contained in 4NAS in 80% of the patients. There was an overlap of 80% among both groups. [52] Numerous studies have addressed the role of AS as an alternate/additional staging procedure to improve the accuracy with respect to SLNB and vice versa [Table 1].
Table 1: Studies elucidating the role of AS and SLNB

Click here to view

Macmillan et al., from 'Nottingham Breast Unit', studied 200 patients (T1-2/ N0) and directly compared SLNB using hot node technique (lymphoscintigraphy) with four-node axillary sampling (4NAS-Edinburgh technique). SLN was identified in 191 patients (96%). When compared with SLNB, 4NAS failed to identify metastasis in one patient (2%). On the contrary, SLNB failed to identify metastasis in eight (14%) patients in whom 4NAS detected axillary lymph node metastasis and hence under-staged the axilla. They concluded that SLNB performed using radiolabeled colloid has no advantage over 4NAS when nodes are assessed by standard histological technique. They affirmed that SLNB for breast cancer may have little to offer four-node-samplers. [52] But this study has been criticized for its faulty design. The authors have compared the two, non-standard axillary staging procedures. The authors should have performed the ALND in each of two groups of patients to find out the false negative nature of either technique (SLNB and 4NAS). [62] Similarly, a comparative Japanese study (Sato et al.) of 206 patients of operable breast cancer undergoing SLNB and four-node sampling procedure (Edinburgh technique) showed that the accuracy and sensitivity of 4NAS (98 and 96%) was comparable to that of SLNB (99 and 98%) respectively. The study concluded that 4NAS can be considered an alternate safe and easy procedure for axillary staging. [57]

Hoar et al., and Lumachi et al., attempted to evaluate whether that additional axillary sampling over and above SLNB improves the false negative rate of SLNB. [53],[54] In addition, Hoar et al., investigated whether woman with positive SLN and no further disease in axilla could be identified by additional AS and therefore spared ALND. Sixty-seven combined SLNB+AS procedures were performed in 66 patients followed by axillary dissection (Level II). Additionally sampled nodes were documented on intraoperative palpation if they were clinically suspicious (AS-S=12) or not (AS-NS=43). By performing an additional sample in these 12 (18.5%) cases based on clinical suspicion (AS-S), three of the four false negative SLN results were avoided, reducing the false negative rate result from 14.3 to 3.6%. Sampling of non-suspicious nodes (AS-NS) in the remaining 43 cases did not avoid the fourth false-negative case. However, the benefit of additional sampling was only seen in those cases with larger tumors (≥ 3 cm) and clinically suspicious nodes (n=12). SLNB alone was found to be inaccurate in the presence of suspicious nodes found intraoperatively and additional sampling of clinically suspicious non-SLNs improves the accuracy and avoids potential false negative results. However, in SLN-positive patients, AS is unreliable in predicting those patients with no further disease in the axilla. [32],[53] Lumachi et al., randomized 112 patients in two groups (SLNB alone, n= 55 and SLNB+AS, n= 57), to find out the usefulness of AS in combination with SLNB in improving the sensitivity of SLNB. They concluded that a combination of SLNB+AS can reduce the false-negative rate of SLNB and improve the sensitivity (73.7% to 90.0%) and accuracy (90.9% to 94.7%). [54]

Agarwal et al., and Gui et al.,[55],[56] while studying SLNB vs. AS found that there is no additional benefit of AS if SLN node is identified, while Chetty et al., concluded that 4NAS improves the accuracy of SLN. [58] Sato et al., found equivalent results between the two groups. [57] Ishikawa et al., did blue dye-assisted 4NAS and found both methods to be complementary and showed improved accuracy of the combined method. [59],[60]

Motomura et al.,[61] performed three axillary lymph node sampling following SLNB to predict the status of nonsentinel nodes in patients with sentinel node metastases with promising results [Table 1]. In a validation study, (intraoperative study of 40 breast cancer patients) at our institute (AIIMS, New Delhi), we tried to find out patients with only positive SLN, (extrapolation of sentinel lymph mapping concept) by injecting blue dye in the SLN (identified by combined blue dye and radioisotope injection). Nodes found upon further mapping were called "Station II nodes". SLNs (Station I nodes) were successfully identified in 98% (39/40) patients. Of the 17 patients with a positive SLN, eight (47%) patients had no further positive nodes in the axilla, nine (53%) patients had additional metastasis in nonsentinel lymph nodes upon completion of ALND. Station II nodes were identified in 76% (13/17) patients with a positive SLN. Station II nodes accurately predicted the status of the remaining axilla in 92% patients (12/13). [63] A large European multicenter, ALMANAC trial randomized patients to SLNB versus ALND or AS for various outcomes; arm morbidity, quality of life, resource costs and for local recurrence in the axilla. [34],[64] Data on comparison between AS and SLNB is not yet available. [65]

 » Comment Top

Axillary clearance (complete or modified) is the gold standard of staging axilla in breast cancer. However, the morbidity associated with it is avoidable, especially in node-negative patients. In patients with clinically negative axilla sentinel lymph node biopsy is the standard of care. However, the blue dye recommended for sentinel node biopsy is not commercially available in India. The hand-held gamma probe is still very expensive and nuclear medicine facilities are not available at many centers across our country. In spite of not being precisely anatomical, AS is a simple technique not needing special training or equipment and hence can be a reasonable alternative to sentinel node biopsy especially in situations where SLNB is not feasible because of varied reasons. There seems to be a role for AS when SLN is not identified while examining the axilla and when there is previous history of excision biopsy of tumor (draining lymphatics are divided and alternate channels open). When facilities are available for SLNB, it seems reasonable to complement the SLNB with AS to improve the accuracy of staging the axilla. Accurate prediction of axilla by 4NAS in case of node-positive axilla, in our opinion, seems to be justified in early-stage tumors (clinically T1-2/N0), since with larger tumors, more tumor burden will overwhelm the axillary lymphatics leaving room for inadequate treatment and understaging of axilla as appears from the studies mentioned in this paper.

 » References Top

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