Original article

New anatomical classification 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 (L’Institut du Sein), 7 Avenue Bugeaud, 75116 Paris, France Correspondence to: Dr K. B. Clough (e-mail: [email protected])

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 classification 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 98·2 per cent of patients the axillary SLN was located medially, alongside the LTV, either below the second ICBN (zone A, 86·8 per cent) or above it (zone B, 11·5 per cent). In only four patients (1·8 per cent) was the SLN located laterally in the axilla. Conclusion: Regardless of the site of the tumour in the breast, 98·2 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 26 August 2010 in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.7217

Introduction axilla (Berg’s level I and II, below and behind the pectoralis minor muscle) is described. The anatomical classification Sentinel lymph node (SLN) biopsy has gradually replaced is based on the intersection of two constant anatomical axillary dissection for small invasive carcinomas, and landmarks in the middle of Berg’s level I: vertically, the indications for this procedure are increasing1–7. Although lateral thoracic tributary of the axillary vein (LTV) and, SLN biopsy has reduced the rate of complications horizontally, the second intercostobrachial nerve (ICBN). associated with axillary dissection, some patients still These two structures form the basis of four different axillary present with chronic arm pain or even lymphoedema8–13. zones16. A secondary aim was to identify, using the same Clinical trials have shown that lymphoedema occurs in classification, the association, if any, between the location 5–7 per cent of patients after SLN biopsy14,15, and chronic of the tumour in the breast and that of the SLN in the axilla. 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 Methods the morbidity associated with the technique but also for teaching purposes. All patients with stage I breast cancer (T1/T2 N0) or ductal The primary aim of this study was to determine the carcinoma in situ (DCIS) who underwent SLN biopsy position of the SLN in the axilla and to demonstrate that localization between January 2005 and October 2006 at the the location is not random, as the flow of lymph from the Paris Breast Centre (L’Institut du Sein) were considered for breast follows a predetermined route. To achieve this aim, the study. Patients requiring preoperative chemotherapy a new anatomical classification of the lower part of the or hormonal therapy and those with a history of previous

 2010 British Journal of Surgery Society Ltd British Journal of Surgery 2010; 97: 1659–1665 Published by John Wiley & Sons Ltd 1660 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 fine- needle aspiration cytology; only patients with negative findings were included in the study. Using anatomical landmarks, the lower part of the axilla (Berg’s level I and the lower part of Berg’s level II) was divided into four anatomical zones to localize the SLN. The B intersection between the LTV (vertically) and the second D ICBN (horizontally) is a constant anatomical landmark in the centre of Berg’s level I16–21 (Fig. 1). These two structures form a cross that creates four zones. Zone A is A the area adjacent to the LTV, extending from the lower C 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 Berg’s 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 a90° abduction position; the base of the axillary pyramid is positioned laterally with its apex at Berg’s level III. Zones Fig. 2 Schematic representation of the lower axilla. Zones A and A and B are adjacent to the LTV. B, and zones C and D form the medial and lateral parts of the To determine the association between the location of the axilla respectively SLN in the axilla and the site of the tumour, the breast was divided into nine sectors: retroareolar (RA), upper outer SLN localization was performed using either patent blue quadrant (UOQ), lower outer quadrant (LOQ), lower dye, technetium-99m nanocolloid tracer, or both, injected inner quadrant (LIQ), upper inner quadrant (UIQ), the into the peritumoral area. The technetium-99m-labelled junction of the upper quadrants (JUQ), the junction of the rhenium sulphide tracer (Nanocis; CIS Bio International, outer quadrants (JOQ), the junction of the lower quadrants Saclay, France) was administered the day before the (JLQ) and the junction of the inner quadrants (JIQ). procedure. Two syringes, each containing 60 MBq (0·2ml) tracer, were injected under ultrasonographic guidance, one at the superficial and the other at the deep pole of the tumour. Lymphoscintigraphy was performed 2 h later. A handheld γ probe was used for counts at the breast injection site, the SLN and the axillary background. The blue dye (2 ml bleu patente´ V sodique 2·5 per cent; Laboratoires 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 first SLN was located. In patients who received only the nanocolloid γ Fig. 1 Intraoperative photograph of the axilla demonstrating the tracer, the probe was used to guide the dissection straight constant intersection of the lateral thoracic vein and the second to the SLN without disturbing the surrounding tissues. intercostobrachial nerve, landmarks for the anatomical The probe was used to check the identified nodes before classification and after excision (in situ and ex vivo). All blue and/or

 2010 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2010; 97: 1659–1665 Published by John Wiley & Sons Ltd Location of the sentinel node in the axilla 1661

radioactive axillary nodes were sampled to reduce the rate Table 2 Number of patients in relation to location of the tumour of false-negative interventions. The axillary background in the breast and site of sentinal lymph nodes in the axilla was then mapped to ensure no remaining hot nodes had Tumour been left behind. Any other clinically suspicious non-SLNs Zone A Zone B Zone C Zone D location were excised. According to the authors’ current protocol, · no attempt was made to remove extra-axillary hot nodes, UOQ 80 10 1 0 91 (40 1) UIQ 27 6 0 0 33 (14·5) such as internal mammary nodes. JUQ 24 3 2 0 29 (12·8) The sites of the SLNs were documented in relation to JOQ 16 1 1 0 18 (7·9) the four axillary zones (A, B, C and D). All SLNs were LOQ 16 1 0 0 17 (7·5) · sent for frozen-section examination; patients with positive LIQ 13 1 0 0 14 (6 2) RA 9 2 0 0 11 (4·8) nodes had immediate axillary lymph node dissection JLQ 8 1 0 0 9 (4·0) (ALND). Negative frozen-section specimens were sent JIQ 4 1 0 0 5 (2·2) for histopathological examination, and deferred ALND SLN location 197 (86·8) 26 (11·5) 4 (1·8) 0 (0) was performed in patients with positive nodes. Values in parentheses are percentages. UOQ, upper outer quadrant; UIQ, upper inner quadrant; JUQ, junction of upper quadrants; JOQ, Results junction of outer quadrants; LOQ, lower outer quadrant; LIQ, lower inner quadrant; RA, retroareolar; JLQ, junction of lower quadrants; JIQ, During the study interval, sentinel node localization was junction of inner quadrants; SLN, sentinel lymph node. performed in 242 patients. Both nanocolloid tracer and patent blue dye were used in 113 patients (46·7 per cent); the remaining 129 patients had either the blue dye alone (123 patients, 50·8 per cent) or the nanocolloid tracer alone (6 patients, 2·5 per cent). In 15 patients (6·2 per cent) the SLN could not be identified during the procedure; these patients underwent ALND and were excluded from the study (only five were found to have lymph node metastasis). The remaining 227 patients had a successful SLN biopsy B and were included in the study. Patient demographics and 11·5% tumour staging are shown in Table 1. Table 2 shows the D 0% distribution of patients according to the location of the tumour in the breast and that of the sentinel node in the · A axilla. The mean number of harvested SLNs was 3 5(range 86·8% 1–6). All SLNs were found in Berg’s level I (214 of 227; C 94·2 per cent) or the lower part of Berg’s level II (13 of 1·8% 227; 5·8 per cent).

Table 1 Patient demographics and tumour staging

No. of patients* (n = 227)

Median (range) age (years) 55·2 (29–85) Side of tumour† Fig. 3 Frequency of location of sentinel lymph nodes in relation Right breast 112 (49·3) to the four axillary zones Left breast 115 (50·7) Histological staging† · Tis (DCIS) 33 (14 5) SLNs were located in zone A in 197 patients (86·8 T1a 10 (4·4) T1b 88 (38·8) per cent), in zone B in 26 (11·5 per cent) and in zone C T1c 73 (32·2) in four (1·8 per cent); in no patient was the SLN located T2 23 (10·1) in zone D (Table 2, Fig. 3). Thus, almost all SLNs (223 of N0 227 (100) 227, 98·2 per cent) were in the medial part of the axilla

*Unless indicated otherwise. †Values in parentheses are percentages adjacent to the LTV, in axillary zones A and B. · unless indicated otherwise. T, tumour category; DCIS, ductal carcinoma Fifty-one patients (22 5 per cent) had positive sentinel in situ; N, node category. nodes, identified by frozen-section examination in 18

 2010 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2010; 97: 1659–1665 Published by John Wiley & Sons Ltd 1662 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

In 98·2 per cent of the 227 patients in this prospective study the axillary SLN was located alongside the LTV, either below (axillary zone A, 86·8 per cent) or above (zone B, 11·5 per cent) the ICBN. This anatomical location of the SLN has not previously been demonstrated clinically. Fig. 4 Magnetic resonance image demonstrating the lateral Such information could be a useful adjunct for practising thoracic vein surrounded by lymph nodes 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, 22·5 per cent had metastatic nodes on histological examination, similar to previously reported rates in the much larger Axillary Lymphatic Mapping Against Nodal Axillary Clearance D B (ALMANAC)14, American College of Surgeons Oncology Group (ACOSOG) Z001015 and National Surgical Adjuvant Breast and Bowel Project B-3229 trials. Sentinel

A node biopsy was originally developed to avoid the C morbidity of ALND. However, the morbidity rate associated with SLN biopsy, although significantly 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 6·9 per cent, paraesthesia 8·6 per cent and decreased upper extremity range of motion 3·8 per cent15. Similar complication rates were reported in Fig. 5 Diagram demonstrating the hypothesis that there are two the 515 patients assigned to the SLN biopsy arm of the distinct lymphatic pathways in the axilla: a medial chain draining ALMANAC trial14. In a prospective Swiss multicentre the breast, centred around the lateral thoracic vein and extending study of 659 patients that compared the morbidity of upwards and medially behind the pectoralis minor muscle to SLN biopsy with that of SLN biopsy followed by ALND, level II nodes (zones A and B), and a lateral chain (zones C and 39 per cent of patients in the former group developed at D) draining the arm least one complication (lymphoedema, numbness, impaired shoulder mobility and pain)8. These studies demonstrated patients (7·9 per cent), who had immediate ALND, and that, although SLN biopsy harvests fewer nodes, the by definitive histology in the remaining 33 (14·5 per cent), procedure can still result in significant intermediate- who underwent ALND as a separate procedure. or long-term morbidity. It is therefore imperative to As all patients were injected peritumorally, an attempt investigate the aetiology of these complications as well was made to correlate the location of the SLN in the as to identify potential ways of reducing them. It is possible axilla with the site of the tumour in the breast (Table 2). that the morbidity of SLN biopsy is associated with the Irrespective of the site of the primary in the breast, axillary extent of dissection. Thus, knowledge of the exact location zone A was the commonest location for SLNs, followed of the sentinel node should help to focus the dissection and

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reduce the morbidity of SLN biopsy procedures without two tracers at two different sites (peritumoral and peri- compromising sensitivity. areolar) and found a concordance rate of 94–98 per cent Berg30 used the pectoralis minor muscle to divide the with regard to the location of the SLN36,37. The concept axillary lymph nodes into three levels. The majority of early that the whole breast drains into the same SLN has posi- and screen-detected breast cancers drain primarily to levels tive practical implications: a periareolar injection could be I and II axillary lymph nodes22. The exact location of the used whether or not the tumour is palpable, and regard- SLN in the axilla is, however, difficult to define, as Berg’s less of its location in the breast, as recommended in the levels have never been subdivided anatomically. Therefore, UK New Start sentinel node biopsy training programme. further anatomical classification is needed to facilitate the However, this is still debated, as other investigators have precise location of the SLN. In the present study, the lower demonstrated that, although most of the breast does drain part of the axilla (Berg’s levels I and II) was divided into into the same SLN, different areas can drain into separate four zones based on the crossing of two constant anatomical nodes25,28. Therefore, until definitive evidence is obtained, structures, the LTV and the second ICBN. The LTV is the present authors still inject all patients peritumorally, a constant landmark in Berg’s level I of the axilla (Figs 1 even for non-palpable tumours, which are injected under and 2). It drains the breast laterally, then courses vertically ultrasonographic guidance24. upwards in the axilla to intersect with the second ICBN The present study did not show that different quadrants before joining the axillary vein anterior to the thoracodorsal of the breast drained into different axillary zones; zone vein16–21. The second ICBN is the lateral cutaneous branch A remained the main draining area for all tumours of the second intercostal nerve. It supplies the skin of the irrespective of their location in the breast. It might be second intercostal space at the medial wall of axilla and concluded from these results that there is only one sentinel the skin of the floor of the axilla, as well as the medial node draining the entire breast. Alternatively, the study side of the upper part of the arm. The nerve enters the may have been limited in that the number of tumours axilla by piercing the serratus anterior muscle in the mid- in each quadrant of the breast was not large enough to axillary line. It traverses the axilla obliquely, lying within demonstrate a significant difference in the location of the axillary fat pad where it gives cutaneous branches to the the SLN. floor of the axilla. It then communicates with the medial Only 1·8 per cent of SLNs in the present study were cutaneous nerve of the arm (arising from the brachial located laterally in zone C, the lateral axillary area plexus) and pierces the deep fascia supplying the skin on outside zone A. None was found in zone D, the lateral the medial side of the upper arm17,31–33. axillary area outside zone B. These findings complement The present study has demonstrated that SLNs are nei- emerging information on the association between the ther equally distributed nor randomly scattered in the four lymphatic drainage of the arm and that of the breast38. defined zones of levels I and II of the axilla. Almost all In the past 3 years there has been growing interest in SLNs (98·2 per cent) were located in the medial part of the axillary location of the SLN draining the arm38–42. the axilla (zones A and B) adjacent to the LTV (Fig. 4). The aim of these studies was to preserve the lymphatic This has not been demonstrated previously in a clinical drainage of the arm in patients undergoing ALND and study, and highlights that the breast lymphatics follow the consequently to minimize the risk of lymphoedema. venous drainage. In only one small autopsy study, Pavlista Axillary reverse mapping (ARM) studies have demonstrated and colleagues34 used a similar technique for localization that ARM-specific nodes almost never harbour metastatic and dissection of the SLN. The axilla was divided into involvement from breast cancer. Nos and co-workers38 four zones using the intersection of the thoracoepigastric have demonstrated previously that the dominant node vein (located lateral to the LTV) and the third ICBN as draining the arm is usually situated in the lateral pillar anatomical landmarks (Fig. 2). Despite small numbers, the of the axilla underneath the axillary vein and above the results were similar to those in the present investigation: second ICBN, an area that corresponds to zone D in the 87 per cent of SLNs were located in the lower and upper present study. ventral quadrants of the axilla, which correspond to zones On the basis of observations in the present study and A and B in the present study. those of the ARM studies38–42 it is hypothesized that There is much debate about whether or not the whole there are two distinct lymphatic pathways in the axilla: a breast drains into the same SLN25–28,35. The second aim of medial chain draining the breast, centred around the LTV the present study was therefore to identify the association, and extending upwards and medially behind the pectoralis if any, between the site of the tumour in the breast and the minor muscle to level II nodes (zones A and B), and a location of the SLN in the axilla. Some authors injected lateral chain (zones C and D) draining the arm (Fig. 5).

 2010 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2010; 97: 1659–1665 Published by John Wiley & Sons Ltd 1664 K. B. Clough, R. Nasr, C. Nos, M. Vieira, C. Inguenault and B. Poulet

Thus, during SLN biopsy, attention should be focused on 6 Blanchard DK, Donohue JH, Reynolds C, Grant CS. zone A and, to a lesser degree, on zone B. If the SLN is not Relapse and morbidity in patients undergoing sentinel lymph found in either of these two areas, the authors recommend node biopsy alone or with axillary dissection of breast cancer. that zone A should be palpated carefully for suspicious Arch Surg 2003; 138: 482–487. nodes that are neither hot nor blue. Conversely, it could be 7 LangerI,MartiWR,GullerU,MochH,HarderF,OertliD et al. Axillary recurrence rate in breast cancer patients with argued that any dissection lateral to zones A and B in the negative sentinel lymph node (SLN) or SLN search for the breast SLN is unnecessary and might explain micrometastasis: prospective analysis of 150 patients after the small, but not negligible, risk of arm lymphoedema SLN biopsy. Ann Surg 2005; 241: 152–158. 8,14,15 following breast SLN biopsy procedures . Similarly, 8 Langer I, Guller U, Berclaz G, Koechli OR, Schaer G, Fehr the common practice during axillary SLN biopsy of MK et al. Morbidity of sentinel lymph node biopsy (SLN) removing enlarged palpable non-sentinel nodes could alone versus SLN and completion axillary lymph node be questioned. The majority of these nodes are found dissection after breast cancer surgery: a prospective Swiss in zone D and a systematic excision might explain the multicenter study on 659 patients. Ann Surg 2007; 245: persistence of lymphoedema in large SLN studies, even 452–461. when a small number of nodes has been removed41.On 9 Schijven MP, Vingerhoets AJ, Rutten HJ, Nieuwenhuijzen the basis of the present study it is recommended that, GA,RoumenRM,vanBusselMEet al. Comparison of morbidity between axillary lymph node dissection and unless highly suspicious, lateral dissection and harvesting sentinel node biopsy. 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Commentary

New anatomical classification of the axilla with implications for sentinel node biopsy (Br J Surg 2010; 97: 1659–1665)

This paper represents the first advance in our anatomical appreciation of the pattern of axillary lymphatic drainage in operable breast cancer since the work of John Berg in the 1950s1. Whereas Berg described an anatomical classification

 2010 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2010; 97: 1665–1666 Published by John Wiley & Sons Ltd 1666 K. B. Clough, R. Nasr, C. Nos, M. Vieira, C. Inguenault and B. Poulet

of axillary lymph drainage applicable to the surgical practice of axillary lymph node clearance, Clough and colleagues have described a classification fit for the new era of sentinel lymph node (SLN) biopsy. Although this is a relatively small study, the data show convincingly that in the vast majority of patients with operable breast cancer the SLN will be found medially in level 1 adjacent to the lateral thoracic (central) vein below its intersection by the second intercostobrachial nerve (ICBN), and in the remainder it will be located medially above the level of the second ICBN. I am confident this paper will inspire further studies. If, in addition to predicting the site of the SLN, it becomes possible to predict the location of involved lymph nodes when the sentinel node is involved, a more focused and less radical axillary dissection to remove the disease might be performed. This would be especially valuable in patients with low-volume or micrometastatic disease in the SLN, many of whom have no further disease in the axilla and are therefore exposed to the morbidity of axillary clearance with no additional benefit. In combination with preoperative axillary staging and intraoperative analysis of the sentinel node, this new anatomical classification of the axillary lymphatic system has the potential to minimize axillary, arm and shoulder morbidity for the majority of patients with breast cancer. A few selected patients with advanced axillary disease may still require a full ‘Berg’-type clearance, but extra care when dissecting laterally, particularly close to the origin of thoracodorsal bundle (to latissimus dorsi), may spare even this group some arm morbidity.

S. Nicholson The Breast Unit, York Hospital, Wigginton Road, York YO31 8HE, UK (e-mail: [email protected]) DOI: 10.1002/bjs.7215

Reference

1 Berg JW. The significance of axillary node levels in the study of breast carcinoma. Cancer 1955; 8: 776–778.

 2010 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2010; 97: 1665–1666 Published by John Wiley & Sons Ltd