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Original article

In vivo study of the surgical anatomy of the axilla


A. Khan, A. Chakravorty and G. P. H. Gui
Academic Surgery (Breast Unit), Royal Marsden NHS Foundation Trust, Fulham Road, London SW3 6JJ, UK
Correspondence to: Mr G. P. H. Gui (e-mail: gerald.gui@rmh.nhs.uk)

Background: Classical anatomical descriptions fail to describe variants often observed in the axilla as they
are based on studies that looked at individual structures in isolation or textbooks of cadaveric dissections.
The presence of variant anatomy heightens the risk of iatrogenic injury. The aim of this study was to
document the nature and frequency of these anatomical variations based on in vivo peroperative surgical
observations.
Methods: Detailed anatomical relationships were documented prospectively during consecutive axillary
dissections. Relationships between the thoracodorsal pedicle, course of the lateral thoracic vein, presence
of latissimus dorsi muscle slips, variations in axillary and angular vein anatomy, and origins and branching
of the intercostobrachial nerve were recorded.
Results: Among a total of 73 axillary dissections, 43 (59 per cent) revealed at least one anatomical
variant. Most notable variants included aberrant courses of the thoracodorsal nerve in ten patients
(14 per cent) – three variants; lateral thoracic vein in 12 patients (16 per cent) – four variants; bifid
axillary veins in ten patients (14 per cent); latissimus dorsi muscle slips in four patients (5 per cent); and
variants in intercostobrachial nerve origins and branching in 26 patients (36 per cent). The angular vein,
a subscapular vein tributary, was found to be a constant axillary structure.
Conclusion: Variations in axillary anatomical structures are common. Poor understanding of these
variants can affect the adequacy of oncological clearance, lead to vascular injury, compromise planned
microvascular procedures and result in chronic pain or numbness from nerve injury. Surgeons should be
aware of the common anatomical variants to facilitate efficient and safe axillary surgery.

Presented in part to a meeting of the Association of Surgeons of Great Britain and Ireland, Liverpool, UK, April 2010;
published in abstract form as Br J Surg 2010; 97(Suppl 2): 12–13
Paper accepted 17 February 2012
Published online 16 April 2012 in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.8737

Introduction Despite the frequency of axillary dissection, comprehen-


sive anatomical descriptions of the axilla and the common
In an era in which sentinel lymph node biopsy (SLNB) variants are lacking in standard texts of anatomy and opera-
has become the standard of care, the role of primary tive surgery. A clear understanding of the surgical anatomy
axillary dissection has become confined to the surgical is essential for the surgeon to achieve complete resec-
management of the lymph node-positive axilla identified tion, minimizing morbidity from avoidable injury to easily
by preoperative ultrasound staging and needle sampling, recognizable soft tissue structures. Some recent studies
or a positive SLNB at intraoperative assessment. A have examined the anatomy of individual structures of
node-positive axilla or completion axillary dissection at interest in isolation1 – 9 . However, few investigations have
considered the relationship of the key structures to each
re-exploration following a previously unexpected positive
other, in particular from the viewpoint of the operating
SLNB may pose significant operative technical challenges.
surgeon10 .
In these patients access to achieve complete surgical In this study, the detailed course and anatomical variants
clearance, defining anatomical boundaries and identifying of some of the principal structures in the axilla were
key landmarks to preserve vital structures often become explored in a consecutive series of patients undergoing
more challenging. axillary dissection for stage II or III invasive breast cancer.

 2012 British Journal of Surgery Society Ltd British Journal of Surgery 2012; 99: 871–877
Published by John Wiley & Sons Ltd
872 A. Khan, A. Chakravorty and G. P. H. Gui

Methods There are no studies or texts documenting variation in


LTV drainage into the axillary vein.
Detailed anatomical relationships between key structures
encountered during consecutive axillary dissections were
documented. Axillary dissection was performed en bloc Accessory axillary vein
in conjunction with a mastectomy. In breast-conserving
The axillary vein is a continuation of the basilic vein and
surgery, the operation was performed either through
originates at the lower margin of teres major. One study
the same incision used to access the breast or via a
documented a variant in axillary vein anatomy; 10 per cent
separate axillary incision. A level III axillary dissection
of patients were found to have a double or accessory axillary
was performed, including the nodes medial to pectoralis
vein running in parallel10 .
minor as the apex of the resection specimen.
Data were collected prospectively from surgical findings
immediately after each operative procedure. In particular, Angular vein
the course and relationships of the thoracodorsal (TD)
The angular vein, a tributary of the SSV, was described
pedicle, lateral thoracic vein (LTV), venous drainage of
by O’Rourke and Layt in 19932 ; the angular vein was
the accessory axillary veins and angular vein, latissimus
found to be present in 95 per cent of axillary dissections.
dorsi (LD) muscle slips, and the origins and branching of
Demonstrated to arise from the scapular anastomosis, the
the intercostobrachial nerve (ICBN) were recorded and
angular vein was described to pass superolaterally to join
compared with standard descriptions of axillary anatomy,
the TDV to form the SSV. A subsequent study of 40
as detailed below.
patients by Chan and Tan3 corroborated this description
and found the angular vein to be present in all 40 patients.
Thoracodorsal pedicle
The TD pedicle comprises the TD nerve (TDN), vein Latissimus dorsi muscle slips
(TDV) and artery (TDA). The TDN originates from the
posterior cord of the brachial plexus and innervates the Variation in the attachments of the LD muscle has been
LD muscle. Standard texts describe the TDN as arising documented in anatomical texts and other literature.
beneath the axillary vein medial to the subscapularis vessels. These variants have been described using a range of
As the nerve descends to enter the LD muscle, it crosses terms, most commonly ‘Langer’s axillary arch’, ‘muscular
to lie in front of the artery (which at this level is called axillary arch’ or ‘LD muscle slips’5 – 7,11 . The frequency
the TDA), before passing lateral to the vessels to penetrate of these variant muscle slips is likely to be population-
the LD muscle11,12 . In a study of 100 axillary dissections, dependent; most authors cite a frequency of between 0·25
Kutiyanawala and colleagues10 found a variant in 5 per cent and 13 per cent5 – 7 .
of patients, in whom the TDN was found to arise medial or
posterior to the subscapular vessels and remain in a medial Intercostobrachial nerve origins and branching
or posterior position until entering the LD muscle. This
configuration was also documented by Chan and Tan3 in a The ICBN is a sensory nerve that innervates the posterior
study of 40 axillary dissections. and medial parts of the upper arm and axilla. Textbooks
The TDV courses superiorly on the anterior surface of of anatomy describe the ICBN as the lateral cutaneous
the subscapularis muscle and becomes the subscapular vein branch of the second intercostal nerve (T2), but also
(SSV) before draining into the axillary vein. Textbooks of document that the lateral cutaneous branch of the third
anatomy and operative surgery11 – 18 and other literature intercostal nerve (T3) can contribute to the ICBN12 – 14 .
documented no variants of the TD vessels from what is The standard description of the course of the ICBN within
considered the standard anatomy. the axilla is of a single branch passing from medial to
lateral. Any branching of the ICBN within the axilla is not
well documented11 – 18 .
Lateral thoracic vein
The LTV is a tributary of the axillary vein, which drains Results
the breast, pectoralis major and serratus anterior. The
arrangement usually displayed in standard texts of anatomy Of the 73 axillary dissections performed in this study, 71
and operative surgery shows the LTV draining directly were carried out in women and two in men. There were
into the axillary vein anteromedial to the TD pedicle11 – 18 . 37 right-sided and 36 left-sided axillary dissections. The

 2012 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2012; 99: 871–877
Published by John Wiley & Sons Ltd
Surgical anatomy of the axilla 873

median patient age was 53 (range 32–86) years. Among a into the axillary vein at its posterior–inferior surface. This
total of 73 axillary dissections, 43 (59 per cent) revealed at anatomical site of entry distinguished it from other venous
least one anatomical variant. drainage into this segment of the axillary vein because other
vessels such as the LTV drained into the inferior border
of the axillary vein having coursed superiorly suspended in
Thoracodorsal pedicle
the fat of the axilla anteromedial to the TD pedicle (Fig. 2).
Thoracodorsal nerve
In 63 axillary dissections (86 per cent), the TDN arose Venous anatomy
beneath the axillary vein medial to the subscapularis vessels,
and crossed these vessels to lie in front of the TDA as Lateral thoracic vein
it descended to enter the LD muscle. In seven patients Four variants in the anatomy of the LTV were identified
(10 per cent), the TDN initially originated medially, then and classified into types 1–4 (Fig. 2). In type 1, the
passed posterior to the vessels to lie lateral to them before most commonly encountered variant affecting 61 patients
entering the LD muscle. A less common variant was seen in (84 per cent), the LTV drained directly into the axillary
three patients (4 per cent), in whom the TDN arose medial vein anteromedial to the TD pedicle.
or posterior to the subscapular vessels and remained in a In the type 2 variant, found in seven patients
medial or posterior position until entering the LD muscle (10 per cent), the LTV joined the SSV to form a common
(Fig. 1). pedicle before draining into the axillary vein. The anterior
branch of the pedicle was found to be the LTV and
Relationship of thoracodorsal artery to vein the posterior branch the SSV. The type 3 variant, in
In 68 patients (93 per cent), the TDA coursed posterior to three patients (4 per cent), had a trifurcating branch of the
the TDV with the vein passing from an anteromedial to axillary vein where the central branch was the LTV, the
an anterolateral position. In the remaining five patients medial branch arose from the chest wall or pectoral vein
(7 per cent), the TDA was found to lay posterolateral and the lateral branch rejoined the axillary vein. The rarer
to the vein throughout the entire course (Fig. 1). The type 4 variant, observed in two patients (3 per cent), was
TDV courses superiorly on the anterior surface of the similar to type 3 but without the lateral branch rejoining
subscapularis muscle and becomes the SSV before draining the axillary vein (Fig. 3).

Observed
frequency (%)

Lateral Medial
Cranial Type 1 84 (61 of 73)
AV

TDA SSV LTV

Type 2 10 (7 of 73)
LTV clipped
AV
TDV
SSV LTV
TDN
Type 3 4 (3 of 73)
AV
Arises from chest
wall/pectoral vein
LTV

Fig. 1Right axillary dissection showing a thoracodorsal nerve Type 4 3 (2 of 73)


(TDN) variant. The TDN lies in a posteromedial position to the AV
thoracodorsal vein (TDV) until entering the latissimus dorsi LTV Arises from chest
muscle. The thoracodorsal artery (TDA) lies posterolateral to wall/pectoral vein
the vein through the entire course. The figure also demonstrates
the type 2 variant of the lateral thoracic vein (LTV); the Fig. 2 Diagram demonstrating the four anatomical variants of the
subscapular vein and LTV join to form a common pedicle that lateral thoracic vein (LTV) and their frequency. AV, axillary
drains into the axillary vein vein; SSV, subscapular vein

 2012 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2012; 99: 871–877
Published by John Wiley & Sons Ltd
874 A. Khan, A. Chakravorty and G. P. H. Gui

Cranial
Cranial
AV

Chest wall perforator


LTB AnV

LTV

SSV
ICBN

TDN

Fig. 3Left axillary dissection showing a type 4 lateral thoracic


vein (LTV). The LTV joins the chest wall or pectoral vein to Fig. 4Left axillary dissection showing variant angular vein
form one common pedicle that drains into the axillary vein (AV). (AnV). The thoracodorsal nerve (TDN) arises medial to the
ICBN, intercostobrachial nerve subscapular vein (SSV) and crosses it anteriorly to lie lateral to it.
At this junction the AnV joins the SSV. A second AnV lies
parallel and inferior to the first. By following the AnVs medially,
Axillary vein the long thoracic nerve of Bell (LTB) is identified
On axillary dissection, ten patients (14 per cent) were found
to have a double axillary vein. Of those with a double
Observed
axillary vein, three patients also had variants in at least one
frequency (%)
other venous structure in the axilla.
Lateral Medial
Type 1 74 (54 of 73)
Angular vein
The angular vein was found to be a constant structure,
Type 2 18 (13 of 73)
present in all axillary dissections performed in this study. A
double angular vein was found in 18 patients (25 per cent)
(Fig. 4). The second angular vein, when present, like the
principle angular vein drained into the collateral circulation
Type 3 3 (2 of 73)
of serratus anterior on the lateral chest wall. Irrespective
of the presence of the second angular vein, the TD vessels
continued on their course inferomedially on to the anterior
surface of the LD muscle.
Type 4 3 (2 of 73)

Latissimus dorsi muscle slips


An axillary arch or LD muscle slip was present in four Type 5 3 (2 of 73)
axillary dissections (5 per cent). In two of these patients,
the arch extended from LD to pectoralis major. In one
Fig. 5Diagram showing the branching patterns of the
patient, the muscle arch linked LD to pectoralis minor,
intercostobrachial nerve in the axilla and their frequency
and in the remaining patient the arch connected LD to the
coracoid process.
The ICBN existed as a single branch while in the
axilla in 54 axillary dissections (74 per cent). In 13 patients
Intercostobrachial nerve origin and branchings
(18 per cent), the ICBN divided into two branches while in
In 66 patients (90 per cent) the ICBN originated from T2 the axilla. Three less common variants noted were: a single
alone, in two patients (3 per cent) from T3 alone, and in branch of the ICBN dividing into more than two branches
five patients (7 per cent) it originated from a combination in the axilla (2 patients, 3 per cent); two or more branches
of T2 and T3. merging to form a single branch in the axilla (2 patients,

 2012 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2012; 99: 871–877
Published by John Wiley & Sons Ltd
Surgical anatomy of the axilla 875

3 per cent); and two or more branches merging to form a axillary vein. This could lead to the disruption of venous
single branch, but rebranching again within the axilla to outflow from the LD muscle.
form two or more distal branches (2 patients, 3 per cent) The axillary vein serves as a landmark to define the upper
(Fig. 5). limit in an axillary dissection. One study reported bifid
axillary veins in 10 per cent of patients10 , compared with
14 per cent in the present study. Iatrogenic injury to this
Discussion
structure can cause significant haemorrhage, particularly
As SLNB has become an accepted method for stag- in a bifid system. Inadvertent ligation of the axillary vein
ing the axilla, the role of axillary dissection is usually or its bifid branch can compromise venous outflow from
in the surgical treatment of established node-positive the arm and contribute to postoperative arm swelling or
disease. False-negative tests arising from intraoperative lymphoedema10 .
assessment of the sentinel node occur, and a second The angular vein, a tributary of the SSV, has been
surgical procedure to the axilla after definitive histol- described previously in three smaller studies, and has
ogy is recommended in up to 5 per cent of women19 – 23 . three important clinical applications2 – 4 . First, the angular
In centres where intraoperative assessment of SLNB is vein can be used to define the inferior limit of axillary
not possible, a positive result often leads to the rec- dissection. Second, the long thoracic nerve can be identified
ommendation for a second axillary procedure. Recur- by following the angular vein towards the chest wall.
rent disease in the axilla after failed primary treatment Finally, the TDN can be identified in proximity to the
can also lead to a recommendation for repeat axillary confluence of the angular vein with the TDV in forming
dissection. the SSV2 – 4 . A double angular vein was identified in 18
The second surgical procedure is often more technically patients (25 per cent) in the present study. This is in
demanding. A sound knowledge of the axillary structures contrast to the findings of O’Rourke and Layt2 who
enables the surgeon to approach the complex axillary reported double angular veins in only 5 per cent of patients,
dissection from different directions. In a heavily involved and Chan and Tan3 who did not mention the presence
axilla with nodes in upper level 2 that obscure visualization of double angular veins. The angular vein represents
of the axillary vein, a lateral approach with initial a collateral circulation between the TD and serratus
identification of the TD pedicle can be helpful. anterior systems, and should be preserved to ensure good
Damage to the TD vascular pedicle or the nerve to LD venous drainage from the trunk, especially after LD flap
may restrict the option of a LD flap breast reconstruction, reconstruction.
or for chest wall resurfacing should there be future The presence of LD muscle slips is not a rare
extensive local cancer recurrence. The relationships of variant. Their recognition improves access to the axilla
the TDA to the TDV are of particular relevance to by allowing surgeons to divide these muscle anomalies
the microvascular surgeon as recipient vessels. The less confidently. Lymph nodes lying posterior and lateral
common variant of the TDN described in the present to these unexpected muscle slips could be missed by
study, where the nerve maintains its medial or posterior an inexperienced surgeon. If the axillary muscle arch
relationship to the vessels until entering the LD muscle, is mistakenly thought to be the free edge of the LD
has been reported previously3,10 . The passage of the TDN muscle, the dissection could inadvertently be taken higher
from an initially medial position to posterior to the vessels than the axillary vein resulting in potential injury to the
to lie lateral to them before entering the LD muscle, axillary artery or brachial plexus5 . The unwary surgeon
however, is an original finding. may also damage the TD pedicle if the muscle slips are
The present study recorded four variants of the divided too close to the LD, affecting immediate or delayed
LTV. Although this structure is often divided during reconstructive options.
axillary surgery, with advances in microvascular procedures ICBN division commonly results in sensory loss of the
preservation of the LTV may prove to be a useful tool. floor of the axilla, extending as a strip of numbness down
Chand and colleagues24 described the use of the LTV as a the upper medial arm. ICBN damage can result in pain and
salvage option in a deep inferior epigastric perforator flap paraesthesia, potentially contributing to shoulder stiffness
when the blood supply to the flap was at risk. The type 2 and a prolonged recovery from surgery25 – 28 . The origins
variant of the LTV poses a particular risk for iatrogenic and branching of the ICBN have been shown to be highly
injury by the inexperienced surgeon, who may sacrifice variable8,9 . In the present study only 47 axillas (64 per cent)
what seems to be the LTV but is actually the common conformed to the standard description, with the ICBN
pedicle formed by the SSV and LTV before joining the originating from T2 alone and existing as a single branch in

 2012 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2012; 99: 871–877
Published by John Wiley & Sons Ltd
876 A. Khan, A. Chakravorty and G. P. H. Gui

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9 Loukas M, Hullett J, Louis RG, Holdman S, Holdman D.
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Snapshot Quiz 12/11


Question: What is the diagnosis shown in this laparoscopic image?

The answer to the above question is found at the end of the Your Views section of this issue
of BJS.

Harris AR, McKevitt G, Neill A: Department of Surgery, Daisy Hill Hospital, 5 Hospital Road, Newry, Northern
Ireland, BT35 8DR (e-mail: a.harris@doctors.org.uk)

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 2012 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2012; 99: 871–877
Published by John Wiley & Sons Ltd

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