Original article

New anatomical classication of the axilla with implications for sentinel node biopsy
K. B. Clough, R. Nasr, C. Nos, M. Vieira, C. Inguenault and B. Poulet
The Paris Breast Centre (LInstitut du Sein), 7 Avenue Bugeaud, 75116 Paris, France Correspondence to: Dr K. B. Clough (e-mail: krishna.clough@orange.fr)

Background: The exact anatomical location of the sentinel lymph node (SLN) in the axilla has not

ascertained clinically, but could be useful both for teaching purposes and to reduce the morbidity of SLN biopsy. The aim of the study was to determine the position of the SLN in the axilla and to demonstrate that this location is not random. Methods: A consecutive series of 242 patients with stage I breast cancer (T1/T2 N0) or ductal carcinoma in situ who underwent SLN localization by peritumoral injection were included in a prospective study to map the location of the SLN in the axilla. A new anatomical classication of the lower part of the axilla based on the intersection of two anatomical landmarks, the lateral thoracic vein (LTV) and the second intercostobrachial nerve (ICBN), is described. These two constant elements form the basis of four axillary zones (A, B, C and D). Results: In 982 per cent of patients the axillary SLN was located medially, alongside the LTV, either below the second ICBN (zone A, 868 per cent) or above it (zone B, 115 per cent). In only four patients (18 per cent) was the SLN located laterally in the axilla. Conclusion: Regardless of the site of the tumour in the breast, 982 per cent of SLNs were found in the medial part of the axilla, alongside the LTV. This information should help to avoid unnecessary lateral dissections.
Paper accepted 2 June 2010 Published online in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.7217

Introduction

Sentinel lymph node (SLN) biopsy has gradually replaced axillary dissection for small invasive carcinomas, and indications for this procedure are increasing1 7 . Although SLN biopsy has reduced the rate of complications associated with axillary dissection, some patients still present with chronic arm pain or even lymphoedema8 13 . Clinical trials have shown that lymphoedema occurs in 57 per cent of patients after SLN biopsy14,15 , and chronic postoperative pain and sensory loss in up to 11 per cent8,14 . Knowledge of the precise anatomical location of the SLN in the axilla would be useful not only in reducing the morbidity associated with the technique but also for teaching purposes. The primary aim of this study was to determine the position of the SLN in the axilla and to demonstrate that the location is not random, as the ow of lymph from the breast follows a predetermined route. To achieve this aim, a new anatomical classication of the lower part of the
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axilla (Bergs level I and II, below and behind the pectoralis minor muscle) is described. The anatomical classication is based on the intersection of two constant anatomical landmarks in the middle of Bergs level I: vertically, the lateral thoracic tributary of the axillary vein (LTV) and, horizontally, the second intercostobrachial nerve (ICBN). These two structures form the basis of four different axillary zones16 . A secondary aim was to identify, using the same classication, the association, if any, between the location of the tumour in the breast and that of the SLN in the axilla.
Methods

All patients with stage I breast cancer (T1/T2 N0) or ductal carcinoma in situ (DCIS) who underwent SLN biopsy localization between January 2005 and October 2006 at the Paris Breast Centre (LInstitut du Sein) were considered for the study. Patients requiring preoperative chemotherapy or hormonal therapy and those with a history of previous
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K. B. Clough, R. Nasr, C. Nos, M. Vieira, C. Inguenault and B. Poulet

surgery to the same breast were excluded. All patients with clinically palpable nodes underwent preoperative neneedle aspiration cytology; only patients with negative ndings were included in the study. Using anatomical landmarks, the lower part of the axilla (Bergs level I and the lower part of Bergs level II) was divided into four anatomical zones to localize the SLN. The intersection between the LTV (vertically) and the second ICBN (horizontally) is a constant anatomical landmark in the centre of Bergs level I16 21 (Fig. 1). These two structures form a cross that creates four zones. Zone A is the area adjacent to the LTV, extending from the lower border of the axilla to the second ICBN. Zone B is the area adjacent to the LTV, extending from the second ICBN to the axillary vein; it extends medially under the pectoralis minor muscle (lower part of Bergs level II). Zone C is the lateral axillary area outside zone A. Zone D is the lateral axillary area outside zone B. Fig. 2 is a schematic representation of these four axillary zones with the arm in a 90 abduction position; the base of the axillary pyramid is positioned laterally with its apex at Bergs level III. Zones A and B are adjacent to the LTV. To determine the association between the location of the SLN in the axilla and the site of the tumour, the breast was divided into nine sectors: retroareolar (RA), upper outer quadrant (UOQ), lower outer quadrant (LOQ), lower inner quadrant (LIQ), upper inner quadrant (UIQ), the junction of the upper quadrants (JUQ), the junction of the outer quadrants (JOQ), the junction of the lower quadrants (JLQ) and the junction of the inner quadrants (JIQ).

A C

Fig. 2

Schematic representation of the lower axilla. Zones A and B, and zones C and D form the medial and lateral parts of the axilla respectively

Fig. 1

Intraoperative photograph of the axilla demonstrating the constant intersection of the lateral thoracic vein and the second intercostobrachial nerve, landmarks for the anatomical classication

SLN localization was performed using either patent blue dye, technetium-99m nanocolloid tracer, or both, injected into the peritumoral area. The technetium-99m-labelled rhenium sulphide tracer (Nanocis ; CIS Bio International, Saclay, France) was administered the day before the procedure. Two syringes, each containing 60 MBq (02 ml) tracer, were injected under ultrasonographic guidance, one at the supercial and the other at the deep pole of the tumour. Lymphoscintigraphy was performed 2 h later. A handheld probe was used for counts at the breast injection site, the SLN and the axillary background. The blue dye (2 ml bleu patent V sodique 25 per cent; Laboratoires e Guerbet, Villepinte, France) was injected immediately before the procedure, as soon as the patient had been anaesthetized. Rigorous massaging was performed after injecting the blue dye22 28 . A transverse incision was made at the hairline of the axilla, or on the hotspot in patients who received the radiotracer. Blunt dissection was carried out to identify the blue-stained lymphatic channel, and was initially followed retrogradely towards the breast to ensure that no medial nodes were missed, then distally until the rst SLN was located. In patients who received only the nanocolloid tracer, the probe was used to guide the dissection straight to the SLN without disturbing the surrounding tissues. The probe was used to check the identied nodes before and after excision (in situ and ex vivo). All blue and/or
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Location of the sentinel node in the axilla

radioactive axillary nodes were sampled to reduce the rate of false-negative interventions. The axillary background was then mapped to ensure no remaining hot nodes had been left behind. Any other clinically suspicious non-SLNs were excised. According to the authors current protocol, no attempt was made to remove extra-axillary hot nodes, such as internal mammary nodes. The sites of the SLNs were documented in relation to the four axillary zones (A, B, C and D). All SLNs were sent for frozen-section examination; patients with positive nodes had immediate axillary lymph node dissection (ALND). Negative frozen-section specimens were sent for histopathological examination, and deferred ALND was performed in patients with positive nodes.
Results

Table 2 Number of patients in relation to location of the tumour in the breast and site of sentinal lymph nodes in the axilla Tumour location 91 (401) 33 (145) 29 (128) 18 (79) 17 (75) 14 (62) 11 (48) 9 (40) 5 (22)

Zone A UOQ UIQ JUQ JOQ LOQ LIQ RA JLQ JIQ SLN location 80 27 24 16 16 13 9 8 4 197 (868)

Zone B 10 6 3 1 1 1 2 1 1 26 (115)

Zone C 1 0 2 1 0 0 0 0 0 4 (18)

Zone D 0 0 0 0 0 0 0 0 0 0 (0)

During the study interval, sentinel node localization was performed in 242 patients. Both nanocolloid tracer and patent blue dye were used in 113 patients (467 per cent); the remaining 129 patients had either the blue dye alone (123 patients, 508 per cent) or the nanocolloid tracer alone (6 patients, 25 per cent). In 15 patients (62 per cent) the SLN could not be identied during the procedure; these patients underwent ALND and were excluded from the study (only ve were found to have lymph node metastasis). The remaining 227 patients had a successful SLN biopsy and were included in the study. Patient demographics and tumour staging are shown in Table 1. Table 2 shows the distribution of patients according to the location of the tumour in the breast and that of the sentinel node in the axilla. The mean number of harvested SLNs was 35 (range 16). All SLNs were found in Bergs level I (214 of 227; 942 per cent) or the lower part of Bergs level II (13 of 227; 58 per cent).
Table 1

Values in parentheses are percentages. UOQ, upper outer quadrant; UIQ, upper inner quadrant; JUQ, junction of upper quadrants; JOQ, junction of outer quadrants; LOQ, lower outer quadrant; LIQ, lower inner quadrant; RA, retroareolar; JLQ, junction of lower quadrants; JIQ, junction of inner quadrants; SLN, sentinel lymph node.

D 0%

B 115%

A 868% C 18%

Patient demographics and tumour staging

No. of patients* (n = 227)

Median (range) age (years) Side of tumour Right breast Left breast Histological staging Tis (DCIS) T1a T1b T1c T2 N0

552 (2985) 112 (493) 115 (507) 33 (145) 10 (44) 88 (388) 73 (322) 23 (101) 227 (100)

Fig. 3

Frequency of location of sentinel lymph nodes in relation to the four axillary zones

*Unless indicated otherwise. Values in parentheses are percentages unless indicated otherwise. T, tumour category; DCIS, ductal carcinoma in situ; N, node category.

SLNs were located in zone A in 197 patients (868 per cent), in zone B in 26 (115 per cent) and in zone C in four (18 per cent); in no patient was the SLN located in zone D (Table 2, Fig. 3). Thus, almost all SLNs (223 of 227, 982 per cent) were in the medial part of the axilla adjacent to the LTV, in axillary zones A and B. Fifty-one patients (225 per cent) had positive sentinel nodes, identied by frozen-section examination in 18
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K. B. Clough, R. Nasr, C. Nos, M. Vieira, C. Inguenault and B. Poulet

by zone B. However, tumours located in the upper pole of the breast (UIQ, UOQ and JUQ) appeared to drain more often in zone B (19 of 131, 15 per cent) in comparison with tumours in the lower pole (LIQ, LOQ and JLQ) (3 of 37, 8 per cent).
Discussion

Fig. 4

Magnetic resonance image demonstrating the lateral thoracic vein surrounded by lymph nodes

A C

Fig. 5

Diagram demonstrating the hypothesis that there are two distinct lymphatic pathways in the axilla: a medial chain draining the breast, centred around the lateral thoracic vein and extending upwards and medially behind the pectoralis minor muscle to level II nodes (zones A and B), and a lateral chain (zones C and D) draining the arm

patients (79 per cent), who had immediate ALND, and by denitive histology in the remaining 33 (145 per cent), who underwent ALND as a separate procedure. As all patients were injected peritumorally, an attempt was made to correlate the location of the SLN in the axilla with the site of the tumour in the breast (Table 2). Irrespective of the site of the primary in the breast, axillary zone A was the commonest location for SLNs, followed
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In 982 per cent of the 227 patients in this prospective study the axillary SLN was located alongside the LTV, either below (axillary zone A, 868 per cent) or above (zone B, 115 per cent) the ICBN. This anatomical location of the SLN has not previously been demonstrated clinically. Such information could be a useful adjunct for practising surgeons and teaching purposes, not only to increase the reliability but also to reduce the morbidity of SLN procedures. SLN biopsy has become the standard minimally invasive alternative to ALND in staging patients with clinically node-negative disease. Although all patients in this study had no node involvement clinically, 225 per cent had metastatic nodes on histological examination, similar to previously reported rates in the much larger Axillary Lymphatic Mapping Against Nodal Axillary Clearance (ALMANAC)14 , American College of Surgeons Oncology Group (ACOSOG) Z001015 and National Surgical Adjuvant Breast and Bowel Project B-3229 trials. Sentinel node biopsy was originally developed to avoid the morbidity of ALND. However, the morbidity rate associated with SLN biopsy, although signicantly lower than that of ALND, is not negligible. In the ACOSOG Z0010 trial, which included 4975 patients, the recorded 6-month morbidity rates of SLN biopsy were as follows: proximal lymphoedema 69 per cent, paraesthesia 86 per cent and decreased upper extremity range of motion 38 per cent15 . Similar complication rates were reported in the 515 patients assigned to the SLN biopsy arm of the ALMANAC trial14 . In a prospective Swiss multicentre study of 659 patients that compared the morbidity of SLN biopsy with that of SLN biopsy followed by ALND, 39 per cent of patients in the former group developed at least one complication (lymphoedema, numbness, impaired shoulder mobility and pain)8 . These studies demonstrated that, although SLN biopsy harvests fewer nodes, the procedure can still result in signicant intermediateor long-term morbidity. It is therefore imperative to investigate the aetiology of these complications as well as to identify potential ways of reducing them. It is possible that the morbidity of SLN biopsy is associated with the extent of dissection. Thus, knowledge of the exact location of the sentinel node should help to focus the dissection and
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Location of the sentinel node in the axilla

reduce the morbidity of SLN biopsy procedures without compromising sensitivity. Berg30 used the pectoralis minor muscle to divide the axillary lymph nodes into three levels. The majority of early and screen-detected breast cancers drain primarily to levels I and II axillary lymph nodes22 . The exact location of the SLN in the axilla is, however, difcult to dene, as Bergs levels have never been subdivided anatomically. Therefore, further anatomical classication is needed to facilitate the precise location of the SLN. In the present study, the lower part of the axilla (Bergs levels I and II) was divided into four zones based on the crossing of two constant anatomical structures, the LTV and the second ICBN. The LTV is a constant landmark in Bergs level I of the axilla (Figs 1 and 2). It drains the breast laterally, then courses vertically upwards in the axilla to intersect with the second ICBN before joining the axillary vein anterior to the thoracodorsal vein16 21 . The second ICBN is the lateral cutaneous branch of the second intercostal nerve. It supplies the skin of the second intercostal space at the medial wall of axilla and the skin of the oor of the axilla, as well as the medial side of the upper part of the arm. The nerve enters the axilla by piercing the serratus anterior muscle in the mid-axillary line. It traverses the axilla obliquely, lying within the axillary fat pad where it gives cutaneous branches to the oor of the axilla. It then communicates with the medial cutaneous nerve of the arm (arising from the brachial plexus) and pierces the deep fascia supplying the skin on the medial side of the upper arm17,31 33 . The present study has demonstrated that SLNs are neither equally distributed nor randomly scattered in the four dened zones of levels I and II of the axilla. Almost all SLNs (982 per cent) were located in the medial part of the axilla (zones A and B) adjacent to the LTV (Fig. 4). This has not been demonstrated previously in a clinical study, and highlights that the breast lymphatics follow the venous drainage. In only one small autopsy study, Pavlista and colleagues34 used a similar technique for localization and dissection of the SLN. The axilla was divided into four zones using the intersection of the thoracoepigastric vein (located lateral to the LTV) and the third ICBN as anatomical landmarks (Fig. 2). Despite small numbers, the results were similar to those in the present investigation: 87 per cent of SLNs were located in the lower and upper ventral quadrants of the axilla, which correspond to zones A and B in the present study. There is much debate about whether or not the whole breast drains into the same SLN25 28,35 . The second aim of the present study was therefore to identify the association, if any, between the site of the tumour in the breast and the
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location of the SLN in the axilla. Some authors injected two tracers at two different sites (peritumoral and periareolar) and found a concordance rate of 9498 per cent with regard to the location of the SLN36,37 . The concept that the whole breast drains into the same SLN has positive practical implications: a periareolar injection could be used whether or not the tumour is palpable, and regardless of its location in the breast, as recommended in the UK New Start sentinel node biopsy training programme. However, this is still debated, as other investigators have demonstrated that, although most of the breast does drain into the same SLN, different areas can drain into separate nodes25,28 . Therefore, until denitive evidence is obtained, the present authors still inject all patients peritumorally, even for non-palpable tumours, which are injected under ultrasonographic guidance24 . The present study did not show that different quadrants of the breast drained into different axillary zones; zone A remained the main draining area for all tumours irrespective of their location in the breast. It might be concluded from these results that there is only one sentinel node draining the entire breast. Alternatively, the study may have been limited in that the number of tumours in each quadrant of the breast was not large enough to demonstrate a signicant difference in the location of the SLN. Only 18 per cent of SLNs in the present study were located laterally in zone C, the lateral axillary area outside zone A. None was found in zone D, the lateral axillary area outside zone B. These ndings complement emerging information on the association between the lymphatic drainage of the arm and that of the breast38 . In the past 3 years there has been growing interest in the axillary location of the SLN draining the arm38 42 . The aim of these studies was to preserve the lymphatic drainage of the arm in patients undergoing ALND and consequently to minimize the risk of lymphoedema. Axillary reverse mapping (ARM) studies have demonstrated that ARM-specic nodes almost never harbour metastatic involvement from breast cancer. Nos and co-workers38 have demonstrated previously that the dominant node draining the arm is usually situated in the lateral pillar of the axilla underneath the axillary vein and above the second ICBN, an area that corresponds to zone D in the present study. On the basis of observations in the present study and those of the ARM studies38 42 it is hypothesized that there are two distinct lymphatic pathways in the axilla: a medial chain draining the breast, centred around the LTV and extending upwards and medially behind the pectoralis minor muscle to level II nodes (zones A and
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K. B. Clough, R. Nasr, C. Nos, M. Vieira, C. Inguenault and B. Poulet

B), and a lateral chain (zones C and D) draining the arm (Fig. 5). Thus, during SLN biopsy, attention should be focused on zone A and, to a lesser degree, on zone B. If the SLN is not found in either of these two areas, the authors recommend that zone A should be palpated carefully for suspicious nodes that are neither hot nor blue. Conversely, it could be argued that any dissection lateral to zones A and B in the search for the breast SLN is unnecessary and might explain the small, but not negligible, risk of arm lymphoedema following breast SLN biopsy procedures8,14,15 . Similarly, the common practice during axillary SLN biopsy of removing enlarged palpable non-sentinel nodes could be questioned. The majority of these nodes are found in zone D and a systematic excision might explain the persistence of lymphoedema in large SLN studies, even when a small number of nodes has been removed41 . On the basis of the present study it is recommended that, unless highly suspicious, lateral dissection and harvesting of lateral palpable non-sentinel nodes be avoided. Breast SLNs are not located randomly in the axilla. In order to determine the precise location of the SLN in the axilla, and to harmonize future research, a new anatomical classication of the lower axilla based on the crossing of two constant anatomical structures, the LTV and the second ICBN, is proposed. This classication will be of value to breast surgeons performing SLN biopsy procedures.
Acknowledgements

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The authors declare no conict of interest.

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