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Surg Radiol Anat (2012) 34:159–165

DOI 10.1007/s00276-011-0886-7

ORIGINAL ARTICLE

The anatomy and variations of the internal thoracic


(internal mammary) artery and implications in autologous
breast reconstruction: clinical anatomical study
and literature review
Alice C. A. Murray • Warren M. Rozen •
Alberto Alonso-Burgos • Mark W. Ashton •

Emilio Garcia-Tutor • Iain S. Whitaker

Received: 27 December 2010 / Accepted: 28 September 2011 / Published online: 11 October 2011
 Springer-Verlag 2011

Abstract limit the use of the IT artery in autologous breast recon-


Background The internal thoracic (IT) vessels (otherwise struction. Preoperative imaging with ultrasound or CTA
known as the thoracica interna or internal mammary ves- may provide a clear and accurate method of identifying
sels) are widely used as recipient vessels in autologous these anatomical variations pre-operatively.
breast reconstruction. Despite this, normal and pathological
variations in IT artery architecture have been described, Keywords Free flap  Perforator flap  Reconstructive
and these have the potential to complicate dissection and surgery  Anatomy  Variation
the selection of suitable vessels.
Methods A clinical anatomical study of 240 IT arteries
(120 patients) and review of the literature was undertaken. Background
Participants comprised 120 female patients undergoing
preoperative imaging of the IT artery prior to autologous The internal thoracic (IT) vessels (otherwise known as the
breast reconstruction, 42 with computed tomographic thoracica interna or internal mammary vessels) are widely
angiography (CTA) and 78 with ultrasound. used as recipient vessels in autologous breast reconstruc-
Results There was complete concordance between sur- tion. In fact, they are often preferred to the thoracodorsal
gical and radiological findings. An IT artery was present in (TD) vessels due to their accessibility, ease of manipulation
100% of cases, with a duplicate IT artery in two cases (1% and freedom of flap placement [11, 28]. They are relatively
overall). The position of the IT artery was between two IT spared following irradiation and axillary surgery compared
veins most frequently (71.5% of cases), and was lateral to with the TD vessels [26] and are usually preserved despite
the vein(s) least frequently (6%). There were large IT wide resections during mastectomies [17]. Numerous
perforators from the first and second intercostal spaces in groups have reported success using IT recipient vessels for
87 and 91% of cases, respectively, with the incidence of autologous breast reconstruction, and in particular for
such perforators reducing in the lower spaces. The litera- abdominal wall deep inferior epigastric artery perforator
ture highlighted a range of cadaveric and clinical cases in (DIEP) and transverse rectus abdominis myocutaneous
which there was absence of a patent IT artery, variant (TRAM) flaps and for gluteal artery flaps [3, 11, 28]. This
course or size, and variant relationship to the IT vein. correlates with studies of the IT vessels over the past
Conclusion A range of congenital, pathological and iat- 20 years showing greater relative anatomical consistency
rogenic variants in IT artery anatomy have the potential to than was previously thought, with vessels of adequate
calibre reliably found at the level of the third intercostal
space [1, 3, 13].
A. C. A. Murray  W. M. Rozen (&)  A. Alonso-Burgos  Despite this, a range of normal and pathological varia-
M. W. Ashton  E. Garcia-Tutor  I. S. Whitaker tions in vessel architecture have been described, in par-
Department of Anatomy and Cell Biology, Jack Brockhoff
ticular for the IT artery, and these have the potential to
Reconstructive Plastic Surgery Research Unit, The University
of Melbourne, Grattan St, Parkville, VIC 3050, Australia complicate dissection and the selection of suitable vessels
e-mail: warrenrozen@hotmail.com [1, 8]. Even if relatively uncommon, the unexpected

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finding of an unsuitable IT artery can have profound projection (MIP) and volume rendered technique (VRT)
implications for a particular patient. As such, consideration reconstructions. For duplex ultrasound, a flow value was
of preoperative imaging of the IT vessels has been sug- assigned to the pulsatile arterial flow in order to accurately
gested [9]. Imaging of the recipient site in autologous identify the IT artery.
breast reconstruction can facilitate detailed preoperative A retrospective analysis of prospectively recorded data
planning which may ultimately improve operative success, was undertaken, with surgical and radiological correlation
and as such imaging of the IT arteries preoperatively has performed in each of the 120 cases. Imaging findings
been an increasingly sought technique. Both ultrasound comprised the presence or absence of an ipsilateral IT
(conventional Doppler ultrasound and modern colour artery, its source vessel of origin, its position as the most
duplex ultrasound) and computed tomographic angiogra- medial or lateral structure in the intercostal space (the third
phy (CTA) have each been widely used as non-invasive intercostal space was used as the reference for these mea-
imaging techniques, with CTA more recently shown to surements, being a common site for dissection of the ves-
provide accurate information about arterial architecture, sels in this clinical setting), and the presence of more than
including vessel origin, calibre, course, length and one arterial trunk. Internal mammary perforating arterial
branching patterns [4]. We sought to undertake a clinical branches were also assessed, and the presence of a perfo-
anatomical study of the IT artery and perform a review of rator over 1 mm from any of the first five intercostal spaces
the literature, as a means to assessing the incidence and was recorded. Vessel size was measured as the internal
types of variation in anatomy that exist for the IT artery diameter of each vessel, representing lumen diameter.
and offer some insight into the role for pre-operative
imaging.
Results

Methods In each of the 240 sides (120 patients) in which imaging of


the IT artery and veins was performed, the IT artery was
A clinical anatomical study of the IT artery was undertaken present and visible on imaging, both for ultrasound (78
through the use of preoperative imaging with either CTA or cases; see Fig. 2) and for CTA (42 cases; see Figs. 3, 4, 5).
colour duplex ultrasound (see Fig. 1). Participants com- Furthermore, in all cases there was complete concordance
prised 120 patients undergoing imaging of the IT vessels between surgical and radiological findings.
for the preoperative imaging of recipient site vasculature The primary outcome measures and their results are
prior to breast reconstruction. Patients were all female, shown in Table 1. In all cases an IT artery was present,
spanned the range of ages between 30 and 75, and were of with no cases demonstrating an absence of the IT artery. In
mixed body habitus. All patients consented to the imaging,
with institutional ethical approval prospectively obtained.
For CTA, arterial phase scans were undertaken, in which a
bolus tracking technique was used to identify filling of the
IT artery with contrast as a means to initiate scanning.
These technique provides pure ‘arterial phase’ scans, with
no or minimal venous opacification and therefore confer a
presumed improved accuracy for identifying arterial bran-
ches (by minimizing the risk of confounders due to con-
fusion between arteries and veins). Intravenous contrast
was used in all cases, with no oral contrast used, and
comprised non-ionic iodinated contrast media: Ultravist
370 (Schering, Berlin, Germany) or Omnipaque 350
(Amersham Health, Princeton, USA) Intravenous access
was accessed through a cubital fossa vein, with an
18-gauge cannula and injection performed with a biphasic
power injection pump at a flow rate of 4–6 mL/s. Image
reformatting software was achieved with either Siemens Fig. 1 Computed tomographic angiogram (CTA) of the thoracic
Syngo InSpace (Siemens, InSpace2004A_PRE_19), or vasculature in a patient with coarctation of the aorta, with volume
rendered technique (VRT) reconstruction, demonstrating a dilated
Osirix (OsiriX Medical Imaging Software, GPL Licensing
internal mammary system and clear representation of its communi-
Open Source Initiative). Multi-planar three dimensional cation with the intercostal arteries and its terminal musculophrenic
reconstructions were achieved with maximum intensity and superior epigastric arteries

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Surg Radiol Anat (2012) 34:159–165 161

Fig. 5 Computed tomographic angiogram (CTA) of the thoracic


vasculature, with maximum intensity projection (MIP) axial recon-
struction, demonstrating the internal mammary artery and course of a
third intercostal space perforator through the breast parenchyma

at the lateral sternal border, as the most medial structure,


most lateral structure or location between two IT veins
Fig. 2 Colour duplex ultrasound of the internal mammary vessels, within the intercostal space, the central position between
demonstrating their course through the intercostal and pectoralis major the two veins was the most frequent position (71.5% of
musculature. Reproduced with permission from Rozen et al. [29] cases), while the lateral position was the least frequent (6%
of cases). The presence of major arterial perforators
([1 mm diameter) from each of the first five intercostal
spaces was assessed on imaging, and it was found that there
were usually dominant IT perforators from the first and
second intercostal spaces (occurring in 87 and 91% of
cases, respectively), with the incidence of such perforators
reducing the more caudal the intercostal space from the
second space down, with only 6 and 5% of cases showing
Fig. 3 Computed tomographic angiogram (CTA) of the thoracic such branches in each of the lower two spaces, respectively
vasculature, with volume rendered technique (VRT) reconstruction, (see Table 1).
demonstrating a duplicate internal mammary artery on the right and
single internal mammary artery on the left

Discussion

The internal mammary vessels as recipient vessels were


initially described by Longmire in his paper on microvas-
cular oesophageal reconstruction in 1947 [23] and it was
only in 1980 that Harashina successfully performed anas-
tomosis of the free groin flap to the internal mammary
vessels for breast reconstruction [16]. Shaw et al. presented
a series of ten cases in which he variably used the IT artery
and/or veins as recipient vessels, with seven cases utilizing
the IT artery and four in which the IT vein were used. The
lack of usability was largely due to the fact that the internal
mammary vein was small at the level of the fifth rib and
was a poor match for the larger donor superior gluteal vein
[32]. Feller et al. [10] described suitable IT arteries for
anastomosis, but again described inconsistent venous
Fig. 4 Computed tomographic angiogram (CTA) of the thoracic diameter; reporting: ‘‘the artery might be adequate as a
vasculature, with maximum intensity projection (MIP) axial recon-
struction, demonstrating the internal mammary artery and course of a
recipient vessel…(but) the vein is most often found to be
second intercostal space perforator through the pectoralis major and inadequate as a recipient vein so that the external jugular or
subcutaneous tissues the cephalic vein… is pulled through subcutaneously into
the dissected chest pocket’’.
two cases, however, there was a duplicate IT artery (1% of These previous authors highlighted a perceived lack of
overall cases). In all cases the IT artery arose from the anatomical consistency, however, much of their anatomical
subclavian artery. In terms of the position of the IT artery data was based on a small number of limited cadaveric

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Table 1 Summary of anatomical features of the internal mammary IT artery position at the lateral sternal border
artery as demonstrated on preoperative imaging
Number of trunks of the IMA (n/%) Various distances between the IT artery and lateral sternal
Zero trunks (absent IMA) 0/240 = 0% border have been reported, anywhere from 6 to 24 mm [1,
One trunk 238/240 = 99% 18, 32, 34]. There have been different methods of mea-
Two trunks 2/240 = 1% surement and different points of reference. Glassberg [12]
Location of the IMA at 3rd intercostal space showed with computed tomography that the mean distance
Medial postion—medial to vein(s) 54/240 = 22.5% between the IT vessels on the right was 15.7 and 14.7 mm
Lateral position—lateral to vein(s) 14/240 = 6% on the left. Ninkovic et al., using ultrasound demonstrated
Central position—between veins 172/240 = 71.5%
consistency in the location and large calibre of IT artery at
Presence of perforating branch of the IMA [1 mm in diameter
the third and fourth intercostals space. The mean distance
First intercostal space 209/240 = 87%
to the sternum was 15.35 mm [28]. Hefel et al. [18] in
female cadaveric studies measured a mean distance of
Second intercostal space 219/240 = 91%
14.97 mm on the right and 14.53 mm on the left. Arnez
Third intercostal space 155/240 = 65%
et al. [1] reported an average distance of 14 mm with a
Fourth intercostal space 15/240 = 6%
range of 6–24 mm. The position of the artery relative to the
Fifth intercostal space 13/240 = 5%
IT veins has been scarcely and variably reported. The
current study was able to contribute this data to the liter-
ature, demonstrating that the artery can variably lie
studies. Since then, a number of seminal papers have gone between, lateral or medial to the IT veins.
on to accurately describe the IT vessel anatomy at each
intercostal level. These studies have proved highly IT artery diameter
important, as they have potentiated the utilization of a
recipient site which is seldom scarred from previous sur- The diameter of the IT artery varies at each intercostal
gery and provides great freedom in flap positioning. The level, with a range of 0.99–2.55 mm at the fourth rib where
current study contributes data forming the largest ana- the IT vessels are commonly used [18, 22]. The IT artery
tomical series on this artery in the literature, and highlights tends to be larger on the right than the left [11, 18]. Arnez
the substantial variability in its course. et al. [1] measured the IT artery at the third, fourth and fifth
intercostal spaces and found that the average diameter was
IT artery origin and course 2.8, 2.6 and 2.6 mm, respectively. Feng [11] reported a
diameter of 2.36 ± 0.50 mm at third intercostal space.
The IT artery runs caudally from its origin of the under- Hefel et al. in their cadaveric study found the IT vessels
surface of the first part of the subclavian artery, about 2 cm suitable for anastomosis in all cases as the smallest diam-
above the clavicle. Occasionally the IT artery can have a eter was 0.99 mm and this was substantiated by Doppler
common origin with the thyrocervical trunk, scapular ultrasound measurements. The mean diameter on the right
artery, dorsal scapular artery, thyroid artery or costocervi- was 1.88 mm and the left 1.76 mm [18]. Ninkovic et al.
cal trunk [18]. From there, it passes inferiorly, posterior to [28] demonstrated a mean diameter 1.87 mm.
the respective brachiocephalic vein and medial to the
scalenus anterior muscle. It continues, at a depth ranging The perforating branches of the IT artery
from 17 to 22 mm [6], dorsal to the sternoclavicular joint
and costal cartilage and ventral to the parietal pleura along Direct perforators arise from the IT artery to the breast and
the internal surface of the rib cage. The artery remains skin at each intercostal space, 1–2 cm lateral to the ster-
lateral to the sternal margins. From the third intercostal num, found either superficial or deep to the pectoralis
space, the artery runs between transversus thoracis and the major muscle [13]. IT perforators as recipient sites, first
outer intercostal muscle layers which separates the vessels described in 1999, have recently been seen as a preferable
from the parietal pleura and increases the safety of mam- option to the regional IT vessels [3]. Previous studies have
mary harvest [27]. Between the sixth and seventh costal suggested that IT perforators appear largest in diameter at
cartilage the IT artery divides into superior epigastric and the second, followed by the third intercostal space where
musculophrenic arteries. The mean length of the IT artery the diameter is on average 1 mm (range 0.5–1.5 mm) for
on each side between origin and termination are: right IT the artery and 1.7 mm (range 0.5–3 mm) for the vein,
artery = 18.05 cm and left IT artery = 18.09 cm [22]. The highlighting that anatomical variants are common [13, 17,
IT artery is always accompanied by at least one vein [18]. 31]. The current studies differed from previous studies, in
These findings were matched in the current study. that first or second intercostals space perforators were by

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Surg Radiol Anat (2012) 34:159–165 163

far the largest, and were usually substantially larger than operatively to assess calibre, luminal diameter and calci-
1 mm in diameter. IT perforators have been used suc- fication of the left IT artery in a patient with bilateral
cessfully for DIEA, TRAM and SIEA flaps. Unlike with subclavian stenosis. Arterial complications of thoracic
the IT vessels there is no need to dissect out costal cartilage outlet obstruction are common, these include chronic
or pectoralis major and the IT artery is preserved as an thrombosis of the subclavian artery, distal arterial micro
arterial conduit for future coronary revascularisation [30]. emboli and subclavian aneurysm and subclavian artery
However, dissection of the perforators can be difficult and thrombosis can extend into the origin of the IT artery and
vessels may be unsuitable due to their calibre. compromise its blood flow [36].

The IT vein Iatrogenic changes in the IT artery

The IT vein is also an important consideration in using the Adjunctive radiation treatment is an integral component
IT vessels as a recipient site, as the absence or unsuitability of breast cancer management, with radiation effects
of the IT vein for venous anastomoses necessitated the within the thoracic vasculature of particular importance in
search for a separate recipient vein. Although an analysis cases of delayed breast reconstruction. Possible operative
of the venous anatomy was outside the scope of the current findings in the IT vessels after radiotherapy include peri-
study, variations in the IT vein have been frequently arterial fibrosis, direct damage to arterial walls and IT
reported as the limiting factor in use of the IT vessels as vein wall thickening [34]. Radiotherapy-related scarring
recipients [34]. Such variations include the course, rela- and fibrosis of the IT vessels can result in the unusability
tionship to the IT artery, bifurcation pattern and diameter of IT vessels [11] with reports of complete IT artery
[1, 8]. occlusion post-mastectomy and radiotherapy [15], and
radiation-induced occlusion of the subclavian artery [7].
Anatomical variations in the IT Artery Previous radiotherapy is a documented reason for non-
usage of the IT artery in coronary artery bypass graft
Variations in IT artery properties between different racial (CABG) surgery [21] and IT artery graft patency is lower
groups and gender have been described. The mean diam- after mediastinal irradiation due to fibrosis and scarring
eter of the internal mammary artery is larger in American [5].
females (2.9 mm) as compared with European females In addition to radiotherapy, previous surgery at the
[18]. Compared to Caucasians, Han et al. [14] have shown donor and recipient site in breast cancer patients has the
that in Asians there are differences in the bifurcation pat- potential to significantly alter vascular anatomy. Local
tern of the IT vein. Additionally there are some less vascular morphology and larger source vessels have been
common anatomical variations that may preclude IT vessel shown to be markedly altered after surgery, with both
use, with these including congenital arteriovenous fistulae division of major arterial or venous channels, as well as
between the IT vessels and pulmonary artery [33], and changes in local vessel calibres shown to occur in response
collateralisation from the IT artery to the iliac artery in to surgical delay. These changes are not always predict-
aorto-iliac vascular disease [2]. able, highlights the role for preoperative imaging in
selected cases.
Pathological changes in the IT artery A detailed awareness of individual anatomy preopera-
tively can facilitate selection of suitable IT vessels where
Pathological vascular changes affecting the IT artery have appropriate and guide surgical approach, which may in
the potential to adversely affect flap survival. IT patency turn reduce intra-operative dissection time and surgical
can be altered in vasculitides of medium and large-sized error, as shown in other body regions [35]. Additionally,
vessels. Segmental occlusions of the IT artery and collat- the ability to accurately measure vessel calibre enables
eralisation around these areas have been reported in matching of both donor and recipient sites, which may
Buerger’s disease, and aneurysmal changes and total reduce conversion rates to alternative vasculature [24], or
obstruction as sequelae of Kawasaki disease [19, 20]. subsequent flap complications [11], as a result of diameter
Subclavian stenosis can threaten the adequacy of the IT discrepancy.
artery as a conduit and potentially alter vessel dimensions.
Causes of subclavian stenosis include: thoracic outlet
syndrome, chronic extra-arterial compression, radiation Conclusion
effects, anti-thrombin III deficiency, and/or thrombus of
cardiac origin (such as in atrial fibrillation). Moussa et al. The IT vessels provide a valuable and reliable recipient site
[25] have shown that CTA was successfully used pre- for autologous breast reconstruction. Detailed anatomical

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studies have improved our knowledge and understanding of 14. Han S, Yoon SY, Park JM (2003) The anatomical evaluation of
the origin, course, related structures and dimensions of the internal mammary vessels using sonography and 2-dimensional
computed tomography in Asians. Br J Plast Surg 56(7):684–688
internal mammary artery and veins. However, congenital 15. Hanet C, Marchand E, Keyeux A (1990) Left internal mammary
anatomical variations, as well as pathologic and iatrogenic artery occlusion after mastectomy and radiotherapy. Am J Car-
processes, have the potential to significantly alter vascular diol 65(15):1044–1045
anatomy such that IT artery may become unusable for use 16. Harashina T, Imai T, Nakajima H, Fugino T (1980) Breast
reconstruction with microsurgical free composite tissue trans-
in the setting of autologous breast reconstruction. Preop- plantation. Br J Plast Surg 33(1):30–37
erative imaging with either ultrasound or CTA may provide 17. Haywood RM, Raurell A, Perks AG et al (2003) Autologous free
a clear and accurate method of identifying these anatomical tissue breast reconstruction using the internal mammary perfo-
variations preoperatively. rators as recipient vessels. Br Plast Surg 56(7):689–691
18. Hefel L, Schwabegger A, Ninkovic M et al (1995) IM vessels:
Ethical Approval Institutional Ethical Approval was anatomical and clinical considerations. Br J Plast Surg
obtained prospectively, and conforms to the provisions of the 48(8):527–532
Declaration of Helsinki in 1995. The subject gave informed 19. Hoppe B, Lu JT, Thistlewaite P et al (2002) Beyond peripheral
consent and patient anonymity has been preserved. arteries in Buerger’s disease: angiographic considerations in
thromboangiitis obliterans. Catheter Cardiovasc Interv
57(3):363–366
Conflict of interest None. 20. Ishiwata S, Nishiyama S, Nakanishi S et al (1990) Coronary
artery disease and internal mammary artery aneurysms in a young
woman: possible sequelae of Kawasaki disease. Am Heart J
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