Axillary node clearance for breast cancer
Alastair M Thompson, Senior Lecturer in Surgical Oncology, University of Dundee.
J.R.Coll.Surg.Edinb., 44, April 1999, 111-117

Axillary node clearance is the established operative management for disease control in invasive breast cancer, obtaining prognostic information and influencing postoperative therapy including the choice of breast cancer trials. Axillary node clearance can be defined as clearing the axillary contents bounded by the axillary skin laterally, latissimus dorsi, teres major and subscapularis posteriorly, the lower border of the axillary vein superiorly, pectoralis muscles anteriorly, and the chest wall medially. The levels of axillary nodes are anatomically defined as level one (inferolateral to pectoralis minor), level two (posterior to pectoralis minor) and level three (superomedial to pectoralis minor) (see Figure 1). In reality, these nodes are in continuity with each other but the concept of axillary node levels is useful when discussing the extent of axillary node surgery.

There are alternatives to level one, two and three axillary node clearance for breast cancer. Some surgeons simply excise the lower axillary nodes (level one), others believe, particularly for small or impalpable cancers, that an axillary node sample taking a minimum of 4 nodes (1) is a satisfactory alternative. Most recently the concept of sentinel node biopsy (reviewed by McIntosh and Purushotham in 1998 (2) has been exciting great interest. Current recommendations, by a range of surgical and oncological groups, are that some form of axillary surgery, and hence axillary staging, should be performed in all patients who undergo operative treatment for breast cancer. It is no longer acceptable to ignore the axilla if performing surgery for breast cancer.

Prior to undertaking an axillary clearance, a diagnosis of breast cancer using triple assessment (clinical, radiological, and pathological) should confirm the presence of an invasive carcinoma of the breast. The patient should have had appropriate staging tests (for which there are also a number of guidelines) prior to surgery. The surgeon should obtain informed consent from the patient for axillary node clearance (together with the breast surgery) which should include discussion of the postoperative management and potential complications. The side for operation should be marked prior to surgery with an indelible marker pen. It is useful to tutor the patient in the physiotherapy exercises for the upper limb which restore mobility post-operatively. The patient should also receive deep vein thrombosis prophylaxis, but does not require antibiotics.

The patient should be positioned lying on her back with the arm abducted and placed on an arm board at 90⁰ to the torso. The surgeon and assistant stand either side of the armboard. Some surgeons prefer to place a wedge underneath the ipse-lateral scapula and to tilt the operating table away from the surgeon, thus giving an improved view of the axilla. Alternatively, preparing and draping the arm separately allows subsequent movement of the upper limb (see below) to facilitate axillary clearance.

Patients undergoing breast conservation (wide local excision or quadrantectomy and axillary node clearance) where the tumour is outwith the axillary tail of the breast require a separate incision for the axillary clearance. Under these circumstances the axillary clearance is performed through a skin crease incision resembling a lazy S just inferior to the axillary hairline. The axillary procedure may be performed before the wide local excision to avoid any potential cross contamination by instruments from the tumour site to the axilla.

At the time of mastectomy, the mastectomy wound can be used to access the axillary tail of the breast and the axillary contents, allowing an excellent exposure of the region.

Access is facilitated by the use of retractors, and particularly by moving the separately draped upper limb to allow easy retraction of the pectoralis muscles (see Figure 2).

For axillary clearance (as part of the breast conservation approach) through a lazy S incision, 1cm flaps of the axillary skin superior and inferior to the incision are raised. The anterior margin (adjacent to the lateral border of pectoralis major) and posterior margin (adjacent to latissimus dorsi) of the axillary tail of the breast are identified, and the tail of the breast dissected with ease off the chest wall to allow a digit or sling to be passed around the axillary tail of the breast. The axillary tail of the breast inferiorly is then separated from the axillary contents superiorly either by sharp dissection with haemostasis using diathermy or ligatures or by three or four clamps then ties across the tissue to allow division of the axillary contents from the breast inferiorly.

The axillary skin can then be further dissected from the axillary tail passing superiorly and the clavipectoral fascia divided to bring the dissection on to the lower border of the axillary vein. Using sharp dissection, pledgelet (Lahey "peanut" swab) dissection and haemostasis (with diathermy, ligatures, metal or absorbable clips) the lower margin of the axillary vein is exposed (see Figure 3). At this stage it may be unclear which vessels passing inferiorly from the vein are the neurovascular bundle to latissimus dorsi, (this bundle lies in a more posterior plane), so one should be cautious about ligating or dividing larger vessels. However, there is usually a single substantial venous tributary passing from the axillary contents to the axillary vein which, once the neurovascular bundle to latissimus has been identified, should be ligated and divided.

The axillary contents are dissected free from the lateral border of pectoralis major and the lateral border of pectoralis minor, taking care to preserve the lateral pectoral neurovascular bundle. Next, the axillary contents can be separated from the medial wall of the axilla where the plane of dissection is usually readily apparent and this plane can be pursued posteriorly towards subscapularis and latissimus dorsi and superomedially into the higher levels of the axilla. During this dissection the intercostobrachial nerve (see Figure 4) and other large intercostal branches are identified as they exit from the medial wall of the axilla and pass across the axilla through the axillary contents to supply the cutaneous innervation of the axillary skin, lateral chest wall and the upper arm. The larger nerves measuring 3 or 4 mm in diameter can be readily identified visually and by palpation and may be dissected free from the axillary fat, nodes and breast tissue.

While it is desirable to preserve these nerves to reduce sensory loss of the axillary skin, one prospective randomised study has demonstrated that there is little symptomatic difference in doing so (3), and if there is heavy axillary involvement with metastatic nodes, the cutaneous nerves should be sacrificed. The nerve to serratus anterior (see Figure 4), which lies surprisingly far posteriorly, will be lifted off serratus anterior during the dissection and can be identified and dissected free from the axillary contents and placed back on the serratus anterior muscle. Transection of this nerve supply would result in a winged scapula.

The lateral border of latissimus dorsi provides the lateral extent of the dissection and the axillary tail can be readily followed superiorly along the border of latissimus dorsi as far as the axillary vein. Care should be taken during this phase of the dissection, since the neurovascular bundle to latissimus dorsi (see Figures 3 and 4) may be distracted into the axillary contents. While in some patients the neurovascular bundle to latissimus dorsi may be easily identified inferiorly, in the majority of patients it is safest to dissect out this neurovascular bundle from the axillary vein. This is done by first identifying the nerve (usually medially, artery and vein posteriorly/inferiorly arising from the axillary vein) and following this bundle inferiorly where it is applied to the surface of latissimus dorsi. During this dissection, small branches of the artery and vein will require careful ligation.

By this stage, the mass of axillary tissue, including the upper most tail of the breast, has now been freed from the breast inferiorly, the chest wall medially, latissimus dorsi laterally, and remains attached by a thin leaf of tissue which passes postero-medially between latissimus dorsi and the subscapular muscles posteriorly and the chest wall medially. This should be carefully divided, ensuring that the nerve to serratus anterior and the nerve to latissiums dorsi do not get pulled into the dissection or even transected.

Further dissection of the level one axillary contents from the inferior margin of the axillary vein (again keeping a careful watch on the nerves to serratus and latissimus dorsi), ligating individual tributaries to the vein and lymphatic channels, allows completion of the lower axillary (level one) clearance.

The axillary clearance may now be continued into the pyramidal shaped upper axilla (see Figure 4) posterior to pectoralis minor (level two) and supero-medially to pectoralis minor to where the axillary vein crosses the first rib (level three). During this dissection, small veins, arterial branches and lymphatic channels along the lower border of the axillary vein should be ligated as far medially as the outer border of the first rib. Once again, the dissection between the axillary contents and the chest wall medially through to the tissue plane is readily performed with branches of the intercostal nerves being identified and vascular branches to the axillary contents divided. Anteriorly, the axillary contents may be dissected off the posterior aspect of pectoralis minor avoiding the pectoral neurovascular bundle (although these may be sacrificed) and the dissection continued to take the apical (level three) tissue and nodes contained therein.

Access to level two and three of the axilla can be greatly facilitated by draping the arm separately and positioning the arm (see Figure 2) across the patient to enable easy retraction of the pectoralis muscle and open up the upper axilla. Alternatively, particularly if the arm is not draped separately, some surgeons prefer to excise pectoralis minor muscle by cutting its insertion into the coracoid process of the scapula and excising the whole muscle together with any interpectoral nodes as originally described by Patey. This certainly gives excellent visibility for level 2 and 3 in the axilla. The interpectoral nodes (Rotter's nodes) can, however, be identified and resected separate from the main specimen (some 2% of patient have involvement of these nodes). As a less radical alternative, the pectoralis minor muscle may be retracted laterally using a sling to allow access between the pectoralis major and pectoralis minor muscle and good visualisation of level three may be obtained in this way.

The axillary clearance should be submitted to the pathologist for dissection of the axillary lymph nodes with the apical tissues marked with a ligature. The number of nodes identified varies according to the extent of surgery but particularly according to the diligence of the pathologist; in centres of excellence, the median number of axillary nodes from the clearance of level one, two and three should be in excess of 20 nodes.

The axillary clearance at the time of mastectomy differs from that described above for clearance through a separate axillary incision in the generally improved access to and visibility of the axilla. If the breast is large and cumbersome, it may be detached at the axillary tail before the axillary dissection commences, in a similar manner to that described above in section 3.

Variations in the anatomy of the axilla need to be recognised. (4) The most common variations include a double axillary vein (in up to one third of patients), minor variations in the course of motor nerves in the axilla and additional strands of aberrant muscle.

Haemostasis is ensured during axillary clearance using absorbable ligatures, metal or absorbable clips, diathermy or a combination of these three. Prior to wound closure, haemostasis is inspected and secured. Some surgeons wash out the wound with tumoricidal wash, although the evidence that this is beneficial in vivo is weak. Prior to wound closure a single close system small diameter vacuum drain is inserted to the axilla and drained externally (see Figure 5). The skin closure for a separate axillary wound or mastectomy wound is of the surgeon’s choosing; there appears to be little advantage between different methods of wound closure. A dressing is applied to the wound and then suction applied to the closed-system vacuum drain.

Dissection of levels one, two and three of the axilla greatly facilitates immediate breast reconstruction using the TRAM (transverse rectus abdominis muscle) technique with free pedicle anastomosis or the latissimus dorsi flap (with skin or mini flap without skin) and, indeed, allows excellent access for endoscopically raising a latissimus dorsi flap. Particular care must be taken to avoid handling of or diathermy adjacent to the latissimus and subscapular vessels if they are to be used for reconstruction.

Care should be taken to identify the lower border of the axillary vein. It is all too easy to pass superior to the vein and artery, led astray by the clavipectoral fascia, and head superiorly towards the brachial plexus when initially trying to identify the vein. Palpating the artery (the vein lies below it) and visualising where the axillary vein will join the upper limb are helpful hints. Most patients have a single axillary vein, but two veins are not uncommon. (4)

The nerve to serratus anterior and the nerve to latissimus dorsi require constant vigilance, as they are very easy to distract towards the dissecting scissors. While most surgeons dissect the axillary contents in continuity it is preferable to also remove any residual nodes or tissue that may be reluctant to join the main specimen, particularly tissue adjacent to the latissimus dorsi neurovascular bundle and the interpectoral nodes.

The axillary contents may be sent to the pathologist separated into level one, level two and level three although in practical terms for postoperative decision making, the number of nodes involved with tumour rather than their precise level influences the choice of therapy and entry into breast cancer trials.

The suction drain should remain in situ for up to five days and should be removed at that time or earlier if less than 50 ml per 24 hours has accumulated. The patient may not need to remain hospitalised with the drain in place. (5) Subsequent accumulation of serous fluid can be aspirated using a needle and syringe under aseptic conditions if required. Upper limb and shoulder girdle mobility should be promoted by the use of physiotherapy exercises taught pre-operatively and supplemented by postoperative instructions and an information leaflet. Clearly adequate postoperative analgesia is required and it is often the axillary surgery rather than that to the breast or chest wall, which causes the greater discomfort. Routine antibiotics are not required, unless an implant has been used for breast reconstruction, and skin dressings should be changed as appropriate. If non-absorbable sutures have been used these should be removed after ten days.

Early complications of clearance of axillary tissue at levels one, two and three include damage to the cutaneous nerves of the chest wall and upper limb, (see Table 1) although it is usually possible to preserve these and dissect them free from the axilla at the time of surgery. However, nerves should certainly be sacrificed rather than compromise clearance of an axilla with a heavy disease burden.

Early complications	Late complications
nerve damage haemorrhage and haematoma wound edge necrosis wound infection seroma	upper limb swelling/lymphoedema reduced upper limb mobility axillary disease recurrence

Postoperative haemorrhage and axillary haematoma formation should occur in less than 1% of patients, although subcutaneous bruising is common. Similarly, necrosis or diathermy burns to the wound edges should not occur. Postoperative wound infection of the axillary wound should occur in less than 5% of patients and may be managed using oral antibiotics, together with drainage of any infected seroma, which may have accumulated.

Seroma formation is common after axillary node clearance and the patient should be warned that this may occur after removal of the drain. In the majority of patients the seroma will either resolve spontaneously or require a single aspiration using a needle and syringe through the axillary skin. Repeated aspiration under aseptic conditions may be used to ensure patient comfort.

From one year following surgery, upper limb swelling and lymphoedema may occur and limitation of movement at the shoulder (glenohumeral joint) may be apparent. (6,7) These complications may be minimised by close attention to the extent of the axillary dissection (and in particular following the lower border of the axillary vein and not dissecting lymphatic tissue superior to this) and by the use of upper limb exercises. In the 1970s and 1980s there was a vogue for administering radiotherapy to the axilla following axillary node clearance, and this resulted in 50% or more of patients enduring disabling upper limb oedema.

Even with careful surgery, upper limb swelling may occur and requires experienced nursing and physiotherapy management, including the use of massage, a forearm or whole arm graduated sleeve, pneumatic compression and bandaging.

Lymph node recurrence should not, in theory, occur following surgical clearance of levels one, two and three of the axilla. However, such recurrence in nodes or extranodal tissue does occur rarely (in less than 2% of patients) and may merit excision of the recurrent tumour. It then becomes a difficult decision as to whether the addition of radiotherapy will confer benefit in terms of disease control or result in unacceptable side effects.

With the more recent trend towards neo-adjuvant chemotherapy in patients who often have substantial lymph node involvement, the desired anti-cancer effect of chemotherapy may render the post-chemotherapy axilla more fibrotic and more difficult to dissect.

KEY POINTS

Positioning and access to axilla

Dissection of axillary contents from boundaries of axilla

Preservation of nerve to serratus anterior, neuro-vascular bundle to latissimus dorsi, intercostobrachial nerve, pectoral nerves

Reduction of postoperative morbidity by careful pre-operative, intra-operative and postoperative management

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