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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
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
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
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
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
LTV
SSV
ICBN
TDN
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
the axilla. In 66 patients (90 per cent), the ICBN originated 5 Babu ED, Khashaba A. Axillary arch and its implications in
from T2 alone, in agreement with the findings of Cunnick axillary dissection–review. Int J Clin Pract 2000; 54:
and co-workers8 . Loukas and colleagues9 reported that 524–525.
73 per cent of ICBNs originated from T2 alone, but 6 Jelev L, Georgiev GP, Surchev L. Axillary arch in human:
that 25 per cent were formed by a combination of T2 common morphology and variety. Definition of ‘clinical’
and T3. In Cunnick and co-workers’ investigation, no axillary arch and its classification. Ann Anat 2007; 189:
ICBN arose from T3, whereas 9 per cent originated from 473–481.
a combination of the first intercostal nerve (T1) and T2. 7 Georgiev GP, Jelev L, Surchev L. Axillary arch in Bulgarian
population: clinical significance of the arches. Clin Anat 2007;
Loukas and colleagues reported that 2 per cent of ICBNs
20: 286–291.
originated from T2, T3 and the fourth intercostal nerve.
8 Cunnick GH, Upponi S, Wishart GC. Anatomical variants
In the present study T1 did not contribute to the ICBN.
of the intercostobrachial nerve encountered during axillary
A notable observation in some patients was that, when
dissection. Breast 2001; 10: 160–162.
the fourth lateral intercostal vessels were accompanied by
9 Loukas M, Hullett J, Louis RG, Holdman S, Holdman D.
large intercostal nerves to supply cutaneous sensation to
The gross anatomy of the extrathoracic course of the
the lateral chest wall and axillary floor, a separate ICBN intercostobrachial nerve. Clin Anat 2006; 19: 106–111.
was also identified. It is postulated that these are distinct
10 Kutiyanawala MA, Stotter A, Windle R. Anatomical variants
levels of segmental innervation of the lateral trunk, axillary during axillary dissection. Br J Surg 1998; 85: 393–394.
floor and the medial upper limb. 11 McMinn RMH. Last’s Anatomy Regional and Applied (9th
The ICBN was found to exist as a single branch while in edn). Churchill Livingstone: Edinburgh, 1994.
the axilla in 54 axillary dissections (74 per cent), in contrast 12 Klimberg VS, Townsend CM, Evers BM. Atlas of Breast
to 51 per cent reported by Cunnick and co-workers8 . In Surgical Techniques. Saunders Elsevier: Philadelphia, 2010.
13 dissections (18 per cent) the ICBN divided into two 13 Standring S. Gray’s Anatomy: the Anatomical Basis of Clinical
branches while in the axilla. The frequency of ICBN Practice (40th edn). Churchill Livingstone Elsevier: London,
variants, in terms of both of their origins and their 2008.
branching patterns, may explain why some randomized 14 Moore KL, Dalley AF, Agur AMR. Clinically Orientated
trials comparing division versus preservation of the ICBN Anatomy (6th edn). Wolters Kluwer Lippincott Williams &
have shown no significant difference in paraesthesia or Wilkins: Philadelphia, 2009.
pain29,30 . 15 Sabel MS. Essentials of Breast Surgery. Mosby Elsevier:
Variations in axillary anatomy are common but poorly Michigan, 2009.
described in the literature. Detailed knowledge of the 16 Dixon M. Breast Surgery: a Companion to Specialist Surgical
axillary anatomy facilitates safe and thorough surgery, often Practice (4th edn). Saunders Elsevier: Edinburgh, 2009.
in an axilla previously treated by surgery, radiotherapy or 17 Spear SL, Hammond DC, Robb GL, Willey SC,
in the presence of cancer recurrence. Nahabedian MY. Surgery of the Breast: Principles and Art (2nd
edn). Lippincott Williams & Williams: Philadelphia, 2005.
18 Rintoul RF (ed.). Farquharson’s Textbook of Operative Surgery
Disclosure (8th edn). Churchill Livingstone: Edinburgh, 1995.
The authors declare no conflict of interest. 19 Layfield DM, Agarwal A, Roche H, Cutress RI.
Intraoperative assessment of sentinel lymph nodes in breast
cancer. Br J Surg 2011; 98: 4–17.
References 20 Contractor K, Gohel M, Al-Salami E, Kaur K, Aqel N,
Nigar E et al. Intra-operative imprint cytology for assessing
1 Khatri VP, Hurd T, Edge SB. Simple technique of early
the sentinel node in breast cancer: results of its routine use
identification of the thoracodorsal nerve during axillary
over 8 years. Eur J Surg Oncol 2009; 35: 16–20.
dissection. J Surg Oncol 2001; 76: 141–142.
21 Neal CH, Daly CP, Nees AV, Helvie MA. Can preoperative
2 O’Rourke MG, Layt CW. Angular vein of the axilla and the
anatomy of the subscapular vein important in axillary node axillary US help exclude N2 and N3 metastatic breast cancer?
dissection. Aust N Z J Surg 1993; 63: 396–398. Radiology 2010; 257: 335–341.
3 Chan CY, Tan M. Spatial relations of the angular vein, an 22 Vanderveen KA, Ramsamooj R, Bold RJ. A prospective,
important landmark in axillary nodal dissection. Br J Surg blinded trial of touch prep analysis versus frozen section for
2003; 90: 948–949. intraoperative evaluation of sentinel lymph nodes in breast
4 Tan MP, Ung OA. Surgical approach to the angular vein of cancer. Ann Surg Oncol 2008; 7: 2006–2011.
the axilla: an ‘inverted’ technique of axillary dissection. Breast 23 Motomura K, Nagumo S, Komoike Y, Koyama H, Inaji H.
J 2007; 13: 220–222. Accuracy of imprint cytology for intraoperative diagnosis of
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 877
sentinel node metastases in breast cancer. Ann Surg 2008; intercostobrachial nerve damage following axillary surgery
247: 839–842. for breast cancer. Breast 1998; 7: 209–212.
24 Chand M, Swan MC, Horlock N, Royle G. Preservation of 28 Torresan RZ, Cabello C, Conde DM, Brenelli HB. Impact
the lateral thoracic vein in axillary dissection – its role in of the preservation of the intercostobrachial nerve in axillary
breast reconstruction using the DIEP flap. Breast 2009; 18: lymphadenectomy due to breast cancer. Breast J 2003; 9:
69–70. 389–392.
25 Ponzone R, Cassina E, Tomasi Cont N, Biglia N, 29 Abdullah TI, Iddon J, Barr L, Baildam AD, Bundred NJ.
Sismondi P. Decreasing arm morbidity by refining axillary Prospective randomized controlled trial of preservation of
surgery in breast cancer. Eur J Surg Oncol 2009; 35: 335–338. the intercostobrachial nerve during axillary node clearance
26 Freeman SR, Washington SJ, Pritchard T, Barr L, for breast cancer. Br J Surg 1998; 85: 1443–1445.
Baildam AD, Bundred NJ. Long term results of a randomised 30 Salmon RJ, Ansquer Y, Asselain B. Preservation versus
prospective study of preservation of the intercostobrachial section of intercostal-brachial nerve (IBN) in axillary
nerve. Eur J Surg Oncol 2003; 29: 213–215. dissection for breast cancer – a prospective randomized trial.
27 Maycock LA, Dillon P, Dixon JM. Morbidity related to Eur J Surg Oncol 1998; 24: 158–161.
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