Common and Rare Collateral Pathways in Aortoiliac Occlusive Disease: A Pictorial Essay

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1 Vascular and Interventional Radiology Pictorial Essay Hardman et al. Collateral Pathways in ortoiliac Occlusive Disease Vascular and Interventional Radiology Pictorial Essay Rulon L. Hardman 1 Jorge E. Lopera 1 Rex. Cardan 2 Clayton K. Trimmer 3 Shellie C. Josephs 3 Hardman RL, Lopera JE, Cardan R, Trimmer CK, Josephs SC Keywords: angiography, blood circulation, collateral pathway, CT scanner, Leriche syndrome, x-ray DOI: /JR Received September 29, 2010; accepted after revision February 23, Department of Radiology, University of Texas Health Science Center in San ntonio, 7703 Floyd Curl Dr, MC 7800, San ntonio, TX ddress correspondence to R. Hardman (hardmanr@uthscsa.edu). 2 Department of Radiation Oncology, University of Louisville, James Graham rown Cancer Center, Louisville, KY. 3 Department of Radiology, University of Texas Southwestern, Dallas, TX. WE This is a Web exclusive article. JR 2011; 197:W519 W X/11/1973 W519 merican Roentgen Ray Society Common and Rare Collateral Pathways in ortoiliac Occlusive Disease: Pictorial Essay OJECTIVE. The development of collateral pathways for arterial blood flow is common in the presence of atherosclerotic occlusive disease of the abdominal aorta and iliac arteries. The collateral pathways are divided into systemic-systemic and systemic-visceral pathways. MDCT is commonly used to evaluate aortic stenosis and the resulting collateral pathways. CONCLUSION. Common and rare arterial collateral pathways are reviewed by 3D volume-rendered CT images. Visceral and lower extremity arterial embryology is reviewed. ortoiliac occlusive disease is most frequently a chronic condition related to the deposition of atherosclerotic plaque at the level of the aortic bifurcation. Other causes of abdominal aortic occlusion include less common entities, such as acute occlusion related to embolus or occlusion related to vasculitis, such as Takayasu arteritis. The prevalence of the disease is unknown because many patients are asymptomatic as a result of the development of rich collateral networks [1, 2]. Symptoms of aortoiliac occlusive disease may range from calf claudication to the more classic Leriche syndrome of impotence, bilateral buttocks claudication, diminished femoral pulses, and aortic occlusion [3]. The advent of MDCT allows less-invasive assessment of aortoiliac occlusive disease over classic angiography. In a metaanalysis of MDCT including 20 studies of 957 patients, the sensitivity was 95% and specificity was 96% for stenosis greater than 50% [4]. The identification of arterial collateral pathways is clinically significant for proper anatomic interpretation of CT images, surgical planning, and avoiding morbidity from vascular injury. few notable collateral pathways require reporting by the radiologist because they can change surgical management. The Winslow pathway has been described in multiple reports as showing iatrogenic damage to the pathway due to the failure to recognize this artery as a collateral source of blood supply to the lower extremities [5, 6]. Using the internal mammary artery for coronary artery bypass surgery in a patient who is dependent on this artery for lower extremity arterial flow can cause lower extremity claudication. The superficial course of this artery may also put it at risk to be inadvertently cut during transverse abdominal surgery [7]. The gonadal artery collateral pathway may be theoretically ligated during renal and scrotal surgeries, thus compromising lower extremity vascularity. Collateral pathways may be seen as direct end-to-end anastomosis of arteries, also referred to as inosculation, or via small branching networks of arterioles. fter reading this pictorial essay, the reader should be aware of the common and rare collateral pathways seen in aortoiliac occlusive disease. Two dominant collateral pathways are seen. The first involves connections between systemic vessels (Fig. 1). The second involves connections between visceral and systemic arteries (Fig. 2). The systemic-systemic collateral pathways include the lumbar (Fig. 3), intercostal (Fig. 4), deep circumflex iliac, internal thoracic (Fig. 5), inferior epigastric, and obturator arteries (Fig. 6). These pathways derive from the embryologic segments of the dorsal aorta. Distal abdominal aorta occlusion tends to collateralize through systemic-systemic pathways [2]. The second main group of collateral pathways involves visceral-visceral or visceral-systemic pathways. The visceral branches derive from ventral and lateral branches of the aorta. The ventral pathways include the celiac truck, superior mesenteric artery, and inferior mesenteric artery (Fig. 7; Fig. S7, supplemental video, can be viewed from the information box in the upper right corner of this article). Unusual pathways can arise from lateral branches via JR:197, September 2011 W519

2 Hardman et al. the renal or gonadal arteries (Fig. 8; Fig. S8, supplemental video, can be viewed from the information box in the upper right corner of this article.) The visceral arteries tend to become more prevalent as the aortic occlusive disease extends cephalad along the aorta, approaching the level of the renal arteries [2]. Embryology The embryologic development of the abdominal and lower extremity arteries allows collateralization flow. The rudimentary arterial supply is divided into the ventral, lateral, and dorsal components. The embryologic ventral system develops into the celiac trunk, superior mesenteric artery, and inferior mesenteric artery; the dorsal system develops into the inferior epigastric arteries, internal thoracic arteries, and lumbar arteries; and the lateral system develops into renal and gonadal arteries (Fig. 9). Systemic-systemic collateral pathways arise from connections of the embryonic dorsal arterial system. These arteries start as somatic branches from the dorsal aorta. The arteries later divide into the intercostal arteries in the thorax and the lumbar arteries in the abdomen. The dorsal arterial branches coalesce anteriorly to form a longitudinal vessel, which transverses the anterior body. These branches later form the internal mammary artery superiorly and inferior epigastric artery inferiorly with potential connections between the two arteries. series of arteries arises from the ventral aspect of the paired dorsal aorta. These arteries initially feed the yolk-sac in the embryo. These arteries are known as the omphalomesenteric arc during the embryonic development and feed both the yolk-sac and primitive gut. s the yolk-sac and gut are divided, the gut becomes associated with the mesentery. The separate omphalomesenteric arcs then fuse with the natural fusion of the dorsal aortas to form a single abdominal aorta. Three trunks namely the celiac, superior mesenteric, and inferior mesenteric arteries develop from the omphalomesenteric arc along the ventral aorta. The arteries shift caudal with the development of the fetus. common origin allows communication between the different trunks and their branches and even fusion of two trunks, as seen in patients with a common celio-superior mesenteric trunk. Early in embryonic development, two arteries develop laterally from the dorsal aorta. These vessels are associated with the mesonephros and will progress to feed the urogenital organs, including the gonadal and renal arteries. ecause these vessels share a common origin, there are varying degrees of communication of the gonadal and renal arteries with the left gonadal artery, typically arising from the left renal artery and the right gonadal artery, with variant anatomy arising from the abdominal aorta, renal arteries, or even adrenal arteries. CT ngiography Method The use of an MDCT scanner is necessary to follow a single contrast bolus injection the entire length of an extremity [8]. scanner with four or more rows of detectors is required to provide adequate imaging speed. t our institution, we use the following protocol on a 64-MDCT scanner (rilliance 64, Philips Healthcare): the tube voltage is set at the standard CT setting of 120 kvp with a variable tube current of 300 m. Images are acquired at a pitch of with a rotation of 1.0 second, FOV of 350 mm, and acquisition of mm and are reconstructed at 0.67 mm 0.67 mm. Nonionic isoosmolar contrast is injected at a rate of 5 ml/s for a total of 150 ml. CT angiography images are evaluated at a 3D workstation, because the collateral pathways may be more easily followed as volume-rendered (VR) and 3D reconstructions. We used both TerraRecon (TerraRecon) and Vitrea (Vital Images) systems to evaluate the cases in this review. VR images, maximumintensity projections (MIPs), and multiplanar reformations are useful in addition to the axial images to determine the length and extent of aortoiliac occlusion and to identify collateral pathways [9]. In one trial, VR images showed greater accuracy in detecting occlusions in small vessels, with a trend toward significance in mm vessels and statistically improved diagnostic accuracy for vessels mm in diameter [10]. Threedimensional VR images are limited by user experience and proper image optimization. MIPs may be better for evaluating small vessels [9, 10]. Combined approach using axial images, MIPs, and VR images provides the best diagnostic evaluation of anatomy. Conclusion therosclerotic disease is common in the elderly and can lead to occlusion of the aorta and iliac arteries. Collateralization via systemic-systemic and systemic-visceral pathways is observed in aortoiliac occlusive disease. These pathways may be clearly identified and evaluated on imaging methods, with CT angiography providing complete information of the entire aorta and prominent collaterals. The radiologist needs to know the common and unusual collateral pathways to correctly identify the pathways. The radiologist should also be aware of the potential of damaging pathways such as a gonadal pathway or Winslow pathway. The surgeon and patient should be made aware of these pathways and the danger of surgical manipulation of these collateral pathways. References 1. Edwards JE, Clagett OT, Drake RL, Christensen N. The collateral circulation in coarctation of the aorta. Proc Staff Meet Mayo Clin 1948; 23: ron KM. Thrombotic occlusion of the abdominal aorta: associated visceral artery lesions and collateral circulation. JR Radium Ther Nucl Med 1966; 96: Leriche R, Morel. The syndrome of thrombotic obliteration of the aortic bifurcation. nn Surg 1948; 127: Met R, ipat S, Legemate D, Reekers J, Koelemay M. Diagnostic performance of computed tomography angiography in peripheral arterial disease: a systematic review and meta-analysis. JM 2009; 301: Prager RJ, kin GC, inder RJ. Winslow s pathway: a rare collateral channel in infrarenal aortic occlusion. JR 1977; 128: Yurdakul M, Tola M, Özdemir E, ayazit M, Cumhur T. Internal thoracic artery-inferior epigastric artery as a collateral pathway in aortoiliac occlusive disease. J Vasc Surg 2006; 43: Krupski WC, Sumchai, Effeney DJ, Ehrenfeld WK. The importance of abdominal wall collateral blood vessels: planning incisions and obtaining arteriography. rch Surg 1984; 119: Hallett RL, Fleischmann D. Tools of the trade for CT: MDCT scanners and contrast medium injection protocols. Tech Vasc Interv Radiol 2006; 9: Fishman EK, Ney DR, Heath DG, Corl FM, Horton KM, Johnson PT. Volume rendering versus maximum intensity projection in CT angiography: what works best, when, and why. Radio- Graphics 2006; 26: ddis K, Hopper KD, Iyriboz T, et al. CT angiography: in vitro comparison of five reconstruction methods. JR 2001: Kim J, Won JY, Park SI, Lee DY. Internal thoracic artery collateral to the external iliac artery in chronic aortoiliac occlusive disease. Korean J Radiol 2003; 4: Petru, Elena S, Dan I, Constantin D. The morphology and the surgical importance of the gonadal arteries originating from the renal artery. Surg Radiol nat 2007; 29: W520 JR:197, September 2011

3 Collateral Pathways in ortoiliac Occlusive Disease Fig. 1 Schematic of systemic-systemic pathways. Systemic collateral pathways arise from embryologic dorsal artery. Dorsal artery begins as somatic branches from dorsal aorta. rteries later divide into intercostal arteries, lumbar arteries, internal mammary arteries, and inferior epigastric arteries. This common embryologic origin allows collateralization to occur. Collateral pathways exist between intercostal arteries, lumbar arteries, and iliolumbar arteries with inferior epigastric and deep circumflex arteries. Fig. 2 Schematic of visceral-systemic and visceral-visceral pathways. Series of arteries arises from ventral aspect of paired ventral embryologic aorta. These arteries initially feed yolk-sac of embryo and are known as omphalomesenteric arc. s yolk-sac and gut are divided, gut becomes associated with mesentery. rcs fuse with fusion of aorta and eventually form three trunks namely celiac, superior mesenteric artery (SM), and inferior mesenteric artery (IM). rteries shift caudal with development of fetus. ecause of their common origin, collateral pathways exist between celiac trunk and its divisions, SM, IM, and superior rectal artery. Extent of atherosclerotic disease will determine pathway that will be used. Variations in visceral arterial anatomy allow unusual collateralization pathways. Fig. 3 Systemic-systemic pathway of lumbar artery collateral in 48-year-old man. Lumbar arteries communicate superiorly with intercostal arteries. Inferiorly, lumbar arteries communicate with external iliac artery via deep circumflex iliac artery [2]. In this CT angiography volume-rendered example of lumbar collateral pathways, there is occlusion of abdominal aorta inferior-to-inferior mesenteric artery extending to common iliac arteries. External iliac arteries are small yet patent. Hypogastric arteries fill from retrograde flow. There is reconstitution of internal and external iliac arteries principally through prominent bilateral lumbar arteries through iliolumbar arteries (arrows). Internal iliac flow may also be maintained via iliolumbar arteries (not seen in this example). Fig. 4 Systemic-systemic intercostal artery collateral pathway in 57-year-old man (), 60-year-old woman (), and 54-year-old woman (C). C, Intercostal arteries provide pathway of collateralization in presence of extensive aortic stenosis. Classic example of intercostal artery collateralization is coarctation of thoracic aorta with rib notching from intercostal artery enlargement. Most common levels for intercostal collateralization in abdominal aorta occlusion are at 11th and 12th rib levels. Intercostal arteries eventually communicate with external iliac artery through network of lumbar and iliolumbar arteries (white arrows, ). Three different cases are shown, with varying degrees of complete occlusion of abdominal aorta due to atherosclerosis. These cases show collateralization via prominent intercostal arteries (arrows, and C). Intercostal arteries anastomose with lower extremity via deep circumflex artery. Collateralization via 11th rib intercostal artery is shown ( and C). There is also prominent Winslow pathway (yellow arrows, ). Multilevel intercostal collateralization including 9th, 10th, and 11th rib levels is also seen (). C JR:197, September 2011 W521

4 Hardman et al. Fig. 6 Systemic-systemic obturator artery collateral in 77-year-old man. Various arterial pathways can transverse pelvis. These arteries are small and often difficult to name but are readily visualized on CT angiography. rterial branches are seen from internal iliac artery, external iliac artery, and common femoral artery. Internal iliac artery branches include obturator, internal pudendal, and symphyseal artery branches. Common femoral artery branches seen in these pelvic collateral pathways include medial femoral circumflex artery, deep external pudendal artery, and superficial external pudendal branches. ll of these arteries have variable origins. CT angiography volume-rendered example of pelvis transverse collateral pathway shows severe stenosis of bilateral common iliac arteries, greater on right side. Prominent obturator arteries (white arrows) are shown bilaterally; they anastomose in pelvis, allowing collateralization to contralateral lower internal iliac artery. Prominent inferior epigastric artery (yellow arrow) is seen. Fig. 5 Systemic-systemic internal thoracic artery collateral pathway in 73-year-old woman. and, Internal thoracic artery collateral pathway is one of most reported in literature because of inadvertent surgical ligation during cardiac bypass surgery or laceration during abdominal surgery [5 7]. Internal thoracic artery (internal mammary artery) communicates with inferior epigastric artery. This pathway is also known as Winslow pathway. Pathway is common in severe atherosclerosis, with Winslow pathway being present in 100% of cases with severe atherosclerosis in one series [11]. lthough conventional angiography may fail to reveal this collateral pathway because of abdominal aorta injection CT angiography methods will show opacification of these arteries with contrast agent, yielding reliable visualization of Winslow pathway. CT angiography volume-rendered image () shows anteroposterior projection of Winslow pathway (arrows). Lateral projection of collateral pathway is seen (). W522 JR:197, September 2011

5 Collateral Pathways in ortoiliac Occlusive Disease Fig. 7 Visceral-visceral and visceral-systemic inferior mesenteric artery (IM) collateral pathways in 62-year-old man. Dominant pathway for superior visceral system to connect with systemic circulation is through IM. Occlusion of superior mesenteric artery or celiac trunk with patent IM will show flow from IM through left colic artery and through pathway such as meandering mesenteric artery. Predominant pathway that IM can use to communicate with systemic circulation involves communication between superior rectal artery branches of IM and middle rectal artery branch from internal iliac artery. IM branches can also communicate to systemic circulation through branches of femoral and external iliac arteries. Two pathways that can provide collateralization include superior rectal artery communicating with obturator artery or internal pudendal artery then connecting to common femoral artery via medial femoral circumflex artery and IM branches of superior gluteal artery communicating with deep circumflex iliac artery. dditionally, superior and middle rectal artery branches of IM anastomose with middle sacral artery, allowing additional collateral pathways. CT angiography volume-rendered image shows abdominal aorta in arterial phase in oblique position. Severe atherosclerotic disease is seen in infrarenal aorta, bilateral iliac arteries, and common femoral arteries. There is single common iliac artery stent on right and multiple common iliac artery stents on left. There is occlusion of right common iliac artery. Right external iliac artery fills via branches of internal iliac artery. Internal iliac artery is fed from flow through dilated IM (white arrows) and prominent superior rectal artery (yellow arrow). Network of collateral vessels connects superior rectal artery to right internal iliac artery. See also Figure S7, 3D rendering of IM collateral pathway, in supplemental data online. Fig. 8 Visceral-systemic gonadal artery collateral pathway in 56-year-old man. and, Gonadal and renal arteries arise from anterolateral aorta. Close proximity of branches produces large variance in origins of gonadal artery, with most common orientation being left gonadal artery arising from left renal artery and right gonadal artery arising from aorta. Occasionally, right gonadal artery arises from right renal artery (4.7 14%) [12]. Rare pattern of collateralization can occur in this variant, with collateral pathways arising via cremasteric and pubic branches of inferior epigastric artery. Collateral pathway is important to report because artery could be accidentally ligated during renal and scrotal surgeries. CT angiography volume-rendered images show patient with bilateral common iliac stents and occlusion of right iliac stent (arrows, ). There is collateralization to external iliac artery via prominent right gonadal artery arising from accessory right renal artery (arrows, ). See also Figure S8, 3D rendering of gonadal artery collateral pathway, in supplemental data online. JR:197, September 2011 W523

6 Hardman et al. D Fig. 9 Embryologic development., orta begins as pair of dorsal aortas. Ventral, lateral, and dorsal branches arise from dorsal aorta at each body segment by 23 days., t approximately 30 days, there is fusion of dorsal aorta. Dorsal intersegmental branches connect and evolve to form lumbar and intercostal arteries. Intercostal arteries connect along anterior thorax and abdomen to form internal mammary artery. Lateral branches of aorta feed mesonephros. These arteries later become renal arteries and gonadal arteries. Ventral segmental arteries are paired early in embryologic development. C, y 36 days, ventral arteries fuse to form single arteries. D and E, Majority of ventral segmental arteries fuse and involute to form three visceral branches. Tenth segment forms celiac trunk (D). Thirteenth segment forms superior mesenteric artery (E). Twenty-second segmental branch forms inferior mesenteric artery. Lower extremity arterial supply derives from ischiadic artery. There is fusion of femoral artery and ischiadic arteries to give arterial supply of lower extremity. FOR YOUR INFORMTION The data supplement accompanying this Web exclusive article can be viewed from the information box in the upper right corner of the article at: E C W524 JR:197, September 2011