Introduction

Management of the axilla has been a key aspect of care of breast cancer patients for decades. It is well established from randomised controlled trials, such as the NSABP B-04, that axillary dissection does not improve survival, but the status of the axillary lymph nodes is a prognostic factor and a component of the American Joint Committee on Cancer (AJCC) staging system. Despite the lack of survival benefit, removal of positive lymph nodes can nevertheless provide an element of local control. Given that many patients in the current era present with mammographically detected, node-negative disease, there has recently been considerable interest in de-escalation of axillary surgery. From increased use of sentinel node biopsy (even in patients undergoing neoadjuvant therapy) to avoidance of axillary dissection in patients with only 1-2 positive nodes, and even avoidance of axillary evaluation altogether for elderly patients with favorable tumors, axillary staging of breast cancer patients has evolved to minimise morbidity, without compromising overall care.

Axillary node clearance

Technique

The contents of the axilla lie deep to the clavipectoral fascia, and are divided into three levels, based on their relationship to the pectoralis minor muscle (see Anatomy, Chapter 1 ). Level I is lateral to the muscle and contains the most lymph nodes, and usually the sentinel lymph node(s). Level II nodes lie behind the pectoralis minor, and Level III is medial to it. Axillary clearance aims to remove the lymph nodes and surrounding axillary fat from at least levels I and II. Level III nodes can also be removed if they are thought to be involved at surgery.

Axillary clearance typically involves making a separate incision in the axilla when breast conservation or nipple-sparing mastectomy is performed. In cases of a conventional mastectomy, the axillary clearance can be performed through the lateral extent of that incision. After raising skin flaps, the clavipectoral fascia is incised to enter the axilla proper. The axillary contents are typically mobilised off the chest wall lateral to the pectoralis major muscle using a combination of blunt dissection and ligation of small lymphatics and veins with electrocautery. It can be helpful to have an assistant retract the pectoralis muscle medially. Larger veins and lymphatics should generally be clipped and ligated. The medial pectoral nerve wraps around the lateral edge of the pectoralis major muscle and should be preserved when possible. Other important structures to identify and preserve include the thoracodorsal bundle, which contains an artery, vein and nerve and lies anterior to the latissimus muscle, which they supply. The long thoracic nerve runs along the chest wall and innervates the serratus anterior muscle. Intercostobrachial nerves are located in a more anterior position and run obliquely, providing sensation to the upper inner arm. Finally, the axillary vein is at the top of the field, and is the superior limit for most axillary dissections. At the conclusion of the dissection, one should generally re-examine the cavity for any residual palpable adenopathy, and examine the space between the pectoralis major and minor adjacent to thoraco-acromial vessels for any palpable nodes and remove them.

Most surgeons leave a drain in the axilla after the axillary dissection is completed, to prevent accumulation of serous fluid and blood postoperatively. These can be removed after 24 hours although some prefer them to remain until less than 50 or 30 ml output per day. Patients can be discharged with the drain. Increasingly after axillary dissection the axillary space is being closed by a series of quilting sutures. By using using a barbed continuous suture this decreases the time required to place these sutures and allows multiple small quilts to be placed without tension. After such quilting drains are not always required.

Complications

Axillary dissection has several known complications, including lymphoedema, limitations in postoperative shoulder and arm mobility, prolonged postoperative pain, cording (Mondor’s disease) and paraesthesia. Inadvertent injury to the long thoracic nerve causes winged scapula due to weakness of the serratus anterior muscle. In the case of damage to the thoracodorsal bundle, weakness of the latissimus muscle ensues, with weakness of the arm with respect to extension, adduction and medial rotation. Injury to the intercostobrachial nerve results in sensory deficit in the upper inner arm.

For many patients, lymphoedema is the most dreaded complication, and efforts to reduce the risk and/or modify the course and progression of the disease continue. Generally speaking, the incidence of self-reported lymphoedema after axillary dissection is about 15%. This risk is higher if axillary radiation is administered postoperatively. Several recent studies suggest that subclinical lymphoedema is far more common among patients undergoing axillary surgery than once appreciated. Data from the ALMANAC trial reported 12-month incidence of lymphoedema of 5% with sentinel lymph node biopsy alone versus 13% with axillary clearance. Exercise is not harmful, and in fact, some data suggest that lifting weights may be helpful in reducing lymphoedema. Otherwise, treatment for lymphoedema is generally supportive, with physical therapy, arm strengthening, and stretching; compression garments for the arm and hand may be helpful in severe cases. Further information on lymphoedema management can be found in chapter ….

Mondor’s disease or syndrome, or cording of the axilla and upper arm, is a self-limited, harmless condition. Cording can also be observed running longitudinally down the anterior chest wall, below the breast. It is typically observed within a couple of months after surgery of the breast and/or axilla. It is believed to be caused by thrombosis in subcutaneous veins and ligation of veins after axillary dissection. Patients may experience pain and/or tenderness in the area, but can be reassured that the condition will subside with time. Warm compresses and non-steroidal anti-inflammatory drugs can be helpful.

Shoulder dysfunction and limitations in range of motion may also be observed after axillary dissection. , Rehabilitation with physical therapy, stretching, strengthening, etc. are the mainstay of treatment, although symptoms may persist for at least a year after surgery. The presence of positive axillary nodes and higher body mass index appear to place women at higher risk for dysfunction, and early intervention for those at high risk should be considered.

Less invasive techniques for axillary staging

While axillary clearance, also known as axillary dissection, is clearly efficacious in accurately staging the axilla, it is also associated with significant morbidity ( Table 10.1 ). Axillary sampling (ANS), a forerunner of sentinel node biopsy removes four palpable nodes from Level I in the axilla was compared with axillary node clearance (ANC) in two randomized trial of patients treated with mastectomy and breast conservation. Patients who were node positive after a 4 node sample received axillary radiotherapy (AXRT). In a pooled analysis of two randomised controlled trials after a median follow-up of 19·4 years, there was no difference in breast cancer survival between ANS versus ANC in patients with node-negative disease (hazard ratio (HR) 0·88, 95 per cent c.i. 0·58 to 1·34; P = 0·557), or between ANS + AXRT versus ANC in those with node-positive breast cancer (HR 1·07, 0·77 to 1·50; P = 0·688). Patients having an ANS had a higher risk of axillary recurrence com pared with those who had ANC if node negative (HR 3·53, 1·29 to 9·63; P = 0·014) or node positive (HR 2·64, 1·00 to 6·95; P = 0·049).

Table 10.1
Comparison of morbidity between axillary surgery techniques
Rate of complications
Study Arm No. Lymphoedema Numbness ↓ ROM
Lumachi et al. SLNB
AS
ALND
54
48
50
3.7%
4.2%
16%
Fleissig et al. SLNB
ALND
424
405
7%
14%
8.7%
19%
6.2%
8.4%
Aitken et al. AS + XRT
AS
ALND
28
26
40
32%
8%
20%
57%
8%
15%
Galimberti et al. SLNB
ALND
453
447
3%
13%
12%
18%
3%
8%
Kootstra et al. SLNB
ALND
34
76
0%
28%
18%
26%
Ashikaga et al. SLNB
ALND
2008
1975
16.7%
27.6%
7.5%
30.5%
13.2%
19.0%
ALND, Axillary lymph node dissection; AS, axillary sampling; ROM, range of motion; SLNB, sentinel node biopsy; XRT, radiation therapy.

Decreased range of motion for abduction.

The technique of sentinel node biopsy was described first in the 1950s and popularised in the staging of melanoma, but it was not until the mid-1990s that the technique began to be employed for the staging of breast cancer. The concept was simple – by injecting a radioactive tracer and/or blue dye into the lymphatics draining the breast, one could identify the first (or ‘sentinel’) lymph nodes of the axilla, such that if the tumour metastasised to the axillary lymph nodes, these nodes would be affected first. If the sentinel nodes were negative, the likelihood of further axillary disease would be low and the benefit of axillary clearance minimal. Hence, the technique of sentinel node biopsy could provide an accurate means of staging the axilla, while minimising the morbidity of axillary dissection. Table 10.2 shows data from several large studies in which sentinel node biopsy was followed by axillary dissection. In general, these data demonstrate that sentinel node identification rates have improved over time; the procedure is highly accurate, with false-negative rates predominantly under 10%. The National Surgical Adjuvant Breast and Bowel Project (NSABP) B-32 trial randomised patients who underwent sentinel node biopsy to routine axillary dissection versus axillary node dissection only if the sentinel node was positive. This study found no difference in overall survival, disease-free survival and locoregional recurrence between the two arms.

Table 10.2
Sentinel node biopsy identification, accuracy and false-negative rates
Study No. SLN ID (%) Accuracy (%) False-negative (%)
Giuliano et al. (1996) 174 65 96 12
Giuliano et al. (1997) 107 66 100 0
Guenther et al. (1997) 145 71 88 12
Veronesi et al. (1997) 163 98 98 5
Borgstein et al. (1997) 130 94 99 2
Krag et al. (1998) 443 93 97 11
Nwariaku et al. (1998) 119 81 99 4
Bass et al. (1999) 186 93 99 2
Veronesi et al. (1999) 376 99 96 7
Viale et al. (1999) 155 100 97 7
Schlag et al. (2000) 146 81 93 8
Molland et al. (2000) 103 85 98 5
Haigh et al. (2000) 283 81 99 3
Doting et al. (2000) 136 93 98 5
Tafra et al. (2001) 535 87 96 13
Bergkvist et al. (2001) 498 90 n/a 11
McMasters et al. (2001) 2206 93 97 8
Krag et al. (2001) 145 98 98 4
Quan et al. (2002) 152 93 100 0
Nano et al. (2002) 328 87 94 8
Shivers et al. (2002) 426 86 99 4
Bergkvist et al. (2005) 675 95 n/a 8
Krag et al. (2007) 2807 97 97 10

Targeted axillary dissection

More recently, the concept of targeted axillary dissection (TAD) has become popularized particularly in patients who, prior to neoadjuvant chemotherapy, had a suspicious lymph node on ultrasound that was biopsied, marked and found to be positive. In order to minimize the false negative rate of sentinel node biopsy alone after neoadjuvant therapy targeted axillary dissection aims to remove remove the marked node that was found to be involved at diagnosis as well as any sentinel lymph nodes, after neoadjuvant therapy. A variety of techniques can be used to mark the involved node at diagnosis including metal clips, radioactive seeds, magseeds, radiofrequency tags and Savi scouts.

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