Aortic Stenosis/Occlusion: Collateral Pathways & Collateral

Damage

Poster No.: C-2609

Congress: ECR 2013
Type: Educational Exhibit
Authors: 1 2
V. V. Kamble , S. JAKHERE , S. B. TIBREWALA ; Mumbai,
1 1

2
Maharashtra/IN, MUMBAI/IN
Keywords: Obstruction / Occlusion, Education, CT-Angiography, Vascular,
Arteries / Aorta
DOI: 10.1594/ecr2013/C-2609

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Page 1 of 38
Learning objectives

• To depict various collateral arterial pathways that develop according to the

levels of aortic stenosis/occlusion, with the help of schematic diagrams and
corresponding CT angiographic images.

• To create awareness of these common and rare pathways amongst

radiologists; inorder to identify, assess and indicate their presence to the
surgeon.

Page 2 of 38
Background

Aortic stenosis/occlusion (ASO) is caused by a wide specturm of disorders like

atherosclerosis, Takayasus arteritis, congenital coarctation of aorta, midaortic dysplastic
syndrome and acute conditions like dissection of aorta, embolus, trauma. By far,
atherosclerosis is the most common cause of ASO. Multiple arterial collaterals develop in
chronic aortic affection, to compensate for the reduced blood flow distal to the stenosis.

ASO is a commonly diagnosed condition by catheter angiographic & CT angiographic

studies of the aorta (aortogram). In common imaging practise, systematic and detailed
assesment of ASO is done in terms of

• Loacation of ASO
• Percentage of stenosis
• Mural/ periaortic pathology
• Affection of branch vessels
• Evaluation of ischemic changes in organs
• Cause of ASO
• Presence of collateral blood supply. Here, the question arises - Is the topic
of collateral circulation addressed satisfactorily?

Complete evaluation of ASO requires a careful assessment of the various collateral

pathways that develop according to the level of aortic affection. A thorough knowledge
of the systemic-systemic, visceral-visceral and systemic-visceral collateral pathways is
essential for this purpose. In patients with ASO, concomitant presence of unrelated non-
vascular pathologies requiring surgical intervention is not an infrequent situation. These
conditions futher reinforce the necessicity to assess the collaterals inorder to avoid intra-
operative complications & ischemia.

Page 3 of 38
Fig. 1: Approach to evaluate collateral circulation in aortic stenosis.
References: Dr. Veenita V. Kamble, Topiwala National Medical College, Mumbai/India

Thoracic aortic stenosis/occlusion:

Takayasus arteritis can affect any part of the thoracic aorta, whereas, congenital
coarctation of aorta affects the proximal descending aorta. In thoracic ASO branches of
the subclavian and axillary artery restore/supplement blood supply via intercostal arteries
to the post stenotic segment. The collateral pathways seen are

• Internal thoracic artery(branch of subclavian artery) → intercostal arteries →

post stenotic aorta (Fig. 2 on page )

Page 4 of 38
 Fig. 2: Systemic-systemic collateral pathway in thoracic aortic stenosis/
occlusion
References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

• Vertebral artery(branch of subclavian artery) → anterior spinal artery →

intercostal arteries → post stenotic aorta (Fig. 3 on page )

Page 5 of 38
 Fig. 3: Systemic-systemic collateral pathway in thoracic aortic stenosis/
occlusion
References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

• Dorsal scapular artery (branch of subclavian artery); thracoacromial artery,

lateral thoracic artery, subscapular artery (branches of axillary artery) →
intercostal arteries → post stenotic aorta (Fig. 4 on page )

Page 6 of 38
 Fig. 4: Systemic-systemic collateral pathway in thoracic aortic stenosis/
occlusion
References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

Surgical Implication: Interruption of the internal thoracic artery during coronary artery
bypass graft surgery, damage to the thoracic wall arteries during thoracotomy and
dissection of axillary lymph nodes in breast malignancy can compromise the blood supply
from these collaterals.

Abdominal aortic and/or iliac stenosis/occlusion:

Page 7 of 38
Atherosclerosis characteristically affects the infrarenal aorta and commonly extends to
involve the iliac arteries. Takayasus arteritis can affect any part of the abdominal aorta.
In these scenarios the mesenteric arteries, the Winslow pathway, the haemorrhoidal
arteries, the lower intercostal/subcostal/lumbar arteries are an important source of
collateral supply. The collateral pathways seen are

• Superior mesenteric artery (SMA) → marginal artery → left colic artery →

inferior mesentric artery (IMA) → post stenotic aorta (Fig. 5 on page )
• Inferior mesenteric artery → superior rectal artery → middle/inferior rectal
artery → internal/external iliac artery (Fig. 5 on page )

Fig. 5: Mesentric collateral circulation in abdominal aortic stenosis/occlusion

Page 8 of 38
 References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

• The Winslow pathway: internal thoracic artery → superior epigastric artery

→ inferior epigastric artery → external iliac artery (Fig. 6 on page )

Fig. 6: Winslow pathway: A systemic-systemic collateral pathway in

abdominal aortic and/or iliac artery stenosis/occlusion
References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

• Lower intercostal, subcostal, lumbar arteries → superior gluteal, ilio-lumbar

arteries → internal iliac artery (Fig. 7 on page )

Page 9 of 38
 • Lower intercostal, subcostal, lumbar arteries → circumflex iliac arteries →
external iliac artery (Fig. 7 on page )

Fig. 7: Systemic-systemic collateral pathway in abdominal aortic and/or iliac

artery stenosis/occlusion
References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

Surgical Implication: Intra-abdominal or pelvic surgeries especially of tumours require

a detailed description of adjacent and supplying collateral vessels to avoid intra-operative
complications and ischemia. The Winslow pathway is prone to damage owing to its
superficial and long path. Interruption of the internal thoracic artery during coronary

Page 10 of 38
artery bypass graft, epigastric artery during reconstructive flap surgery and transverse
abdominal incisions have been reported to precipitate acute limb ischemia [6,7].

Surgical & Radiological implication: On the basis of a thorough literature survey Johan
F. Lange et al have emphasized the replacement of the terminologies Riolans arch and
meandering mesenteric artery by the more appropriate and precise term Marginal artery
or Marginal artery of Drummond [3]. Meandering mesenteric artery is an unsuitable term
used to indicate the hypertrophied marginal artery on angiography.

Major aortic branch vessel stenosis/occlusion:

The branches of the aorta may be affected alone or in association with aortic affection.
The spectrum of disorders that cause ASO also cause branch vessel stenosis.

• Subclavian artery stenosis, is associated with collateral flow from

branches distal to the obstruction, thus maintaining upper limb perfusion.
In proximal subclavian stenosis, the post-stenoptic subclavian artery is
reconstituted by retrograde flow from the ipsilateral vertebral artery via the
vertebra-basilar system called the subclavian steal phenomenon. In the
less commonly occuring long-segment occlusions, extending beyond the
origin of the vertebral artery, the collateral circulation is from branches of the
thyrocervical trunk, via the suprascapular-circumflex humeral circulation, and
from the lateral thoracic artery via the intercostal arteries.

• Celiac trunk/ Superior mesenteric artery/Inferior mesentric artery

stenosis:SMA ↔ marginal artery ↔ left colic artery ↔ IMA is an
important collateral pathway in affection of the mesentic vessels( Fig.
5 on page ) . Collateral blood flow from the superior and inferior
pancreaticoduodenal arteries can also occur (Fig. 8 on page ).

Page 11 of 38
Fig. 8: Anastomosis between pancreaticoduodenal arteries: source of
collateral circulation in Celiac artery/SMA stenosis
References: Dr. Veenita V Kamble, Topiwala National Medical College,
Mumbai/India

Page 12 of 38
Fig. 5: Mesentric collateral circulation in abdominal aortic stenosis/occlusion
References: Dr. Veenita V. Kamble, Topiwala National Medical College, Mumbai/India
• Renal artery stenosis is associated with development of collateral arterial
plexus which is formed from branches of the uretric, suprarenal, genital,
lumbar, lower intercostal, inferior phrenic arteries. (Fig. 9 on page )

Page 13 of 38
 Fig. 9: Collateral circulation in renal artery stenosis
References: Dr. Veenita V. Kamble, Topiwala National Medical College,
Mumbai/India

• A worth mentioning condition is that of endovascular aneurysm repair

(EVAR) of descending thoracic aorta leading to post-operative compromise
of a few intercostal arteries. This may hamper flow to the artery of
Adamkiewicz. Post-operatively the left internal thoracic artery, left
thoracodorsal artery have been reported to provide collateral circulation to
the artery of Adamkiewicz via an intercostal artery [8]. Other thoracic wall
arteries & lumbar arteries can also be a source of collateral circulation to this
artery. Thus, collateral circulation plays an important role in post-operative
spinal perfusion, preventing spinal cord ischemia.

Page 14 of 38
Surgical Implication: Owing to the varied origin of the genital arteries and their role
in collateral circulation in renal artery stenosis, it is prone to injury during urogenital
surgeries.

Thus to summarize, collateral circulation in thoracic ASO is dependent on systemic-

systemic collateral pathways; whereas abdominal ASO is dependent on visceral-
visceral, systemic-systemic & systemic-visceral collateral pathways as described earlier.
Systemic-systemic collateral pathways are formed between arteries supplying the body
wall, visceral-visceral collateral pathways are formed between splanchnic arteries and
systemic-visceral collateral pathways are formed between arteries supplying the body
wall and splachnic arteries.

Embryology of the arterial system:

In the fetus the single ventral aortic trunk, 6 pairs of aortic arches, paired dorsal aortas
and their branches undergo series of changes to develop into the adult form of arterial
system.

• The single ventral aortic trunk is divided by a septum to form the two major
arteries - the proximal part of arch of aorta & pulmonary artery.
• The paired aortic arches in contiguity with ventral & dorsal aortic roots form
the proper arch of aorta, innominate artery, proximal internal carotid artery,
proximal external carotid artery, proximal right subclavian artery.
• The paired dorsal aortas unite in the midline to form the descending thoracic
and abdominal aorta.
• Three groups of multiple paired segmental branches develop from the dorsal
aorta: the dorsal (parietal) intersegmental branches, the ventral (visceral)
segmental branches & the lateral (visceral) segmental branches.
• The dorsal intersegmental branches further develop as follows: (a)
Anastomosis between the cervical intersegmental branches → vertebral
th th
artery, (b) the 6 /7 cervical intersegmental artery → left subclavian artery,
(c) the thoracic intersegmental arteries → intercostal arteries, (d) the
th
lumbar intersegmenal arteries → lumbar arteries, (e) the 5 pair of lumbar
intersegmenal arteries → iliac arteries, (f) Longitudinal anastomosis between
the anterior ends of the thoracic and lumbar intersegmental arteries →
internal thoracic artery and epigastric arteries.
• The multiple paired ventral (visceral) segmental arteries fuse in the midline
and loose their paired nature. These arteries develop into the Celiac trunk,
SMA & IMA.
• The lateral (visceral) segmental arteries supply the mesonephros. These
develop into periaortic plexus of vessels to supply the developing urogenital
system, and finally single paired renal and gonadal arteries remain.

Page 15 of 38
Based on the embryological common origin and anastomosis of the dorsal (parietal)
intersegmantal branches, systemic-systemic collaterals develop between arteries
supplying the body wall in ASO. Similarly, visceral-visceral collaterals develop between
mesenteric arteries due to their common origin from the ventral (visceral) segmental
arteries. In renal artery stenosis, a plexus of collaterals from multiple arteries reconstitute
the renal flow which reflects the embryological blood supply of the mesonephros & the
common origin of these arteries from the lateral (visceral) segmental arteries.

Page 16 of 38
Imaging findings OR Procedure details

Catheter angiography is the standard technique for evaluation of the aorta. Multislice CT
is also an excellent tool to evaluate the aorta, especially the collaterals in aortic stenosis.
This is due to the advantage of 2D and 3D reconstruction (Maximum Intensity Projection
images, Volunme Rendered images) in multiple desired views from the scanned data.
Other advantages of CT aortography are visualization of the aortic wall, surrounding
changes, evaluation of organs supplied, rapid imaging time, less invasive, lack of
complications due to arterial catheterization.

CT angiography/aortography was performed using a 64 slice CT scanner followed by

reconstruction of 3D volume rendered and maximum intensity projection images as
desired.

• A 32 year old woman with mastectomy done for left breast malignancy has
features of Takayasus arteritis on CT aortogram. Descending thoracic aortic
stenosis & complete occlusion of infrarenal aorta is seen. (Fig. 10 on page
32 ).

Systemic-systemic collateral pathways have developed to compensate for the thoracic

aortic stenosis.

Systemic-systemic, internal thoracic artery # intercostal arteries collateral circulation is

seen (Fig. 11 on page ).

Fig. 11: Maximum intensity projection & volume rendered images showing collateral
supply from internal thoracic artery (red arrows) to inter-costal arteries (white arrows)

Page 17 of 38
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

Systemic-systemic, subscapular artery # intercostal arteries collateral circulation is seen(

Fig. 12 on page ).

Fig. 12: Maximum intensity projection & volume rendered images showing collateral
circulation between subscapular artery (red arrows in volume rendered image, white
arrow in MIP image) and intercostal arteries (red arrows in MIP image)
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

Prominent dorsal scapular artery is also noted contributing collateral blood flow via
intercostal arteries( Fig. 13 on page ).

Fig. 13: Maximum intensity projection images shows prominent left dorsal scapular
artery(red arrows) which is a source of collateral flow to the thoracic aorta via
intercostal arteries.

Page 18 of 38
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

All three types of collateral pathways: systemic-systemic, visceral-visceral & stytemic-

visceral collaterals have developed to compensate for the infrarenal aortic occlusion.

The IMA & infrarenal aorta are reformed by mesentric collateral circulation (Fig. 14 on
page ).

Fig. 14: Maximum intensity projection & volume rendered images showing reformation
of the IMA(dashed white arrows)and infrarenal aorta by collateral circulation from the
SMA(white arrows) via marginal artery(dashed red arrows).
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

The systemic-systemic, Winslow pathway is developed to restore flow in the iliac arterial
system (Fig. 15 on page ).

Page 19 of 38
Fig. 15: Maximum intensity projection & volume rendered images showing collateral
circulation by the Winslow pathway: Internal mammary artery(white arrows) → superior
& inferior epigastric arteries(red arrows) → external iliac arteries(dashed white arrows).
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

Another systemic-systemic collateral pathway between the lower intercostal arteries and
circumflex iliac arteries is seen restoring flow to the iliac arterial system (Fig. 16 on page
).

Page 20 of 38
Fig. 16: Maximum intensity projection & volume rendered images showing collateral
circulation from the lower intercostal & subcostal arteries(red arrows) to the extenal
iliac artery via the circumflex iliac artery(white arrows)
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

The patient has undergone surgical treatment for breast malignancy and was prone to
surgical damage of the thoracic wall arteries (collateral circulation) during dissection of
axillary lymph nodes (Fig. 17 on page ).

Page 21 of 38
Fig. 17: Axial multislice CT aortography image at the level of mid-thorax: Left sided
mastectomy(white arrows) is done for breast malignancy. Prominent internal mammary
arteries(red arrows) are also seen.
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

• A 60 years old man has atherosclerotic occlusion of the infrarenal abdominal

aorta and proximal left subclavian artery (Fig. 18 on page 32).

The IMA is reformed by the SMA via the marginal artery (Fig. 19 on page ).

Page 22 of 38
Fig. 19: Volume rendered images showing reformation of the IMA(white arrows)
by collateral circulation from the SMA(red arrows) via marginal artery(dashed white
arrows).
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

The iliac arteries were reformed by collateral flow from the systemic-sytemic arterial
pathways (Fig. 20 on page , Fig. 21 on page and Fig. 22 on page )

Page 23 of 38
Fig. 20: Volume rendered image showing collateral circulation from the lower
intercostal & subcostal arteries(red arrows) to the internal iliac artery via the iliolumbar
artery white arrows)
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

Page 24 of 38
Fig. 21: Volume rendered image showing collateral circulation from the lower
intercostal & subcostal arteries(red arrows) to the external iliac artery via the circumflex
iliac artery (white arrows)
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

Page 25 of 38
Fig. 22: Axial multislice CT aortography image at the level of the iliac bones showing
bilateral prominent iliolumbar arteries(white arrows) and prominent right circumflex iliac
artery(red arrow).
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

• A 19year old boy with Takayasus arteritis, has diffuse mild narrowing of the
distal descending thoracic aorta, stenosis of the SMA and left renal artery.
(Fig. 23 on page 33)

The SMA is reformed by collateral flow from the celiac artery via the pancreaticoduodenal
arteries and also by retrograde flow from the IMA via the marginal artery. (Fig. 24 on
page )

Page 26 of 38
Fig. 24: Volume rendered image showing stenosis of the SMA at its origin(red arrow).
Reformation of the SMA(white arrow) by the pancreaticoduodenal arteries(red dashed
arrow) and by retrograde flow from IMA via the marginal artery(dashed white arrow) is
seen.
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

The left renal artery is reformed by a plexus of tiny collateral branches from the genital
artery, periuretric arteries, lumbar arteries, etc. (Fig. 25 on page , Fig. 26 on page
)

Page 27 of 38
Fig. 25: Maximum intensity projection image showing reformation of the renal artery
and a collateral branch(white arrow) from the genital artery(red arrow). A calculus is
present in the lower pole of the kidney.
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN

Page 28 of 38
Fig. 26: Maximum intensity projection images showing renal artery stenosis(red
dashed arrow) with reformation by collateral plexus (red arrows). Genital artery(red
arrowhead) and renal calculus(white dashed arrow) are also seen.
References: Topiwala National Medical college, B.Y.L. Nair Charitable hospital -
Mumbai/IN
The concomitant presence of a renal calculus is also seen. If at all the renal calculus
disease progresses to a stage where surgical intervention is required, the surgeon has
to be warned about these plexus of collateral vessels.

• A 16yrears old girl has bilateral renal artery stenosis and infrarenal aortic
stenosis secondary to Takayasus arteritis.

A plexus of collaterals vessels is reforming the renal artery. (Fig. 27 on page )

Page 29 of 38
•

Fig. 27: Maximum intensity projection and volume rendered images

showing reformation of the renal artery by a prominent collateral from the
inferior phrenic artery (dashed white arrow). Collateral circulation from
periuretric arterial plexus, contribution from the genital artery (white arrow)
and collaterals from the lumbar arteries(red dashed arrow) is also seen. Mild
infrarenal aortic stenosis (red arrowhead) is present.
References: Dr. Veenita V Kamble, Topiwala National Medical College,
Mumbai/India

• An 18year old boy has stenosis of all the aortic arch vessels secondary to
Takayasus arteritis. Distal reformation of both subclavian arteries due to
retrograde flow from the vertebral arteries has occured. Fig. 28 on page
34

Page 30 of 38
•

Fig. 28: Volume rendered image showing stenosis of all the aortic arch
vessels(white arrows) with distal reformation of both subclavian arteries
by retrograde flow from the vertebral arteries(red arrows). Stenosis of
descending thoracic aorta is also seen.
References: Topiwala National Medical college, B.Y.L. Nair Charitable
hospital - Mumbai/IN

Page 31 of 38
Images for this section:

Fig. 10: Maximum intensity projection & volume rendered images of the aorta showing
stenosis of descending thoracic aorta (whit arrows) and occlusion of infrarenal aorta (red
arrows)in a 32 year old woman having Takayasus arterietis.

© Topiwala National Medical college, B.Y.L. Nair Charitable hospital - Mumbai/IN

Page 32 of 38
Fig. 18: Maximum intensity projection & volume rendered images of the aorta showing
atherosclerotic infrarenal aortic occlusion(red arrows)

© Topiwala National Medical college, B.Y.L. Nair Charitable hospital - Mumbai/IN

Page 33 of 38
Fig. 23: Maximum intensity projection image showing diffuse narrowing of dital thoracic
aorta(white arrow) and occlusion of SMA(red arrow) at its origin.

© Topiwala National Medical college, B.Y.L. Nair Charitable hospital - Mumbai/IN

Page 34 of 38
Fig. 28: Volume rendered image showing stenosis of all the aortic arch vessels(white
arrows) with distal reformation of both subclavian arteries by retrograde flow from the
vertebral arteries(red arrows). Stenosis of descending thoracic aorta is also seen.

© Topiwala National Medical college, B.Y.L. Nair Charitable hospital - Mumbai/IN

Page 35 of 38
Conclusion

• Imaging plays an important role not only in evaluating site of aortic stenosis
but also the collateral pathways.

• CT aortography is an excellent tool to assess collateral circulation owing to

the advantage of 2D & 3D reconstruction of images in multiple views.

• A radiologist's keen eye and awareness of these collaterals contributes in

avoiding surgical complications.

Page 36 of 38
References

1. Rulon L. Hardman et al. Common and Rare Collateral Pathways in Aortoiliac

OcclusiveDisease: A Pictorial Essay. AJR 2011; 197:W519-W524
2. Carmen Sebastia et al. Aortic Stenosis: Spectrum of Diseases Depicted at
Multisection CT. RadioGraphics 2003; 23:S79-S91
3. Johan F. Lange et al. Riolan's arch: confusing, misnomer, and obsolete.
A literature survey of the connection(s) between the superior and inferior
mesenteric arteries. The American Journal of Surgery 2007; 193:742-748
4. Hiroki Ando et al. Abnormal collateral arterial systems in Takayasu's
arteritis and Leriche's syndrome evaluated by whole body acquisitionusing
multislice computed tomography. International Journal of Cardiology 2007;
121:306-308
5. R. E. Paul et al. Angiographic Visualization of Renal Collateral Circulation
as a Means of Detecting and Delineating Renal Ischemia. Radiology June
1965; 84:1013-1021
6. Fikri Yapici et al. Limb Ischemia Due to Use of Internal Thoracic Artery in
Coronary Bypass. Asian cardiovascular thoracic annals 2002; 10:254-255
7. William C. Krupski et al. The Importance of Abdominal Wall Collateral Blood
Vessels. Planning Incisions and Obtaining Arteriography. Arch Surg 1984;
119:854-857
8. M. Nakai et al. Thoracodorsal Artery as a Collateral Source to the Artery of
Adamkiewicz After Endovascular Aneurysm Repair for Descending Thoracic
Aortic Aneurysm. European Journal of Vascular and Endovascular Surgery
2009; 37:566-568

Page 37 of 38
Personal Information

Dr. Veenita V. Kamble

Radiology Department

Topiwala National Medical College

Email: vnita_k@yahoo.com

Dr. Sandeep Jakhere

Radiology Department

Topiwala National Medical College

Dr Sunita B. Tibrewala

Head of Radiology Department

Topiwala National Medical College

Page 38 of 38