Multidetector Computed Tomographic Angiography for Optimal Cartography of the Visceral Abdominal Arterial Network: An Extensive Pictorial Review with Emphasis on Common and Uncommon Collateral Pathways, Complications and some Specific Syndromes

Multidetector computed tomographic angiography (MDCTA) is the new gold standard for diagnostic evaluation of the abdominal and/or mesenteric arteries. It is not invasive and provides a 2D and 3D global cartography of all abdominal arteries and that with only a limited amount of contrast media. MDCTA allows the optimal diagnosis of single or multiple arterial stenosis and easily analyses sometimes very complex collateral pathways. It constitutes a major advance to plan the arterial visceral safety of major commonly performed abdominal surgical procedures such as aorto-iliac surgery, endovascular aneurysm repair (EVAR), but also complex pancreatic and gastrointestinal or colonic surgery. It also allows to plan the most optimal strategy for revascularization of the mesenteric system through percutaneous angioplasty, stent placement or surgical bypass. This extensive pictorial review illustrates a large variety of situations which may be found during clinical practise. Single compression or stenosis of each digestive artery, combined and/or complex associations of stenosis and/or compressions of several arteries, secondary complications like aneurysms and classical but also sometimes unusual patterns of collateralization are richly illustrated. Specific syndromes comprising the median arcuate ligament syndrome (MALS) and the Leriche’s syndrome are also discussed.


Introduction
Today the panel of imaging techniques available to investigate abdominal vessels is varied comprising of duplex and color flow Doppler sonography, angio-CT, angio-MRI and conventional angiography (CA). The choice of one technique over another depends on its availability, the clinical circumstances, the degree of emergency but also on the patient's physical characteristics, age and renal function.
Multidetector computed tomographic angiography (MDCTA) today represents the best choice when the purpose of the examination is to quickly and easily obtain optimal global and non-invasive analysis and/or cartography of the abdominal and visceral vessels with all their interconnections. In this context MDCTA represents the new gold standard and outperforms CA. MDCTA has major advantages on CA. First, it is a very fast and non-invasive technique which only requires a limited amount of intravenous contrast media to provide high quality 2D and 3D anatomic images. Then a global cartography of all arteries may be obtained simultaneously, an opportunity that cannot be meet during CA. Multiple successive selective or semi-selective invasive catheterizations would be necessary to obtain such a global analysis of all abdominal vessels during CA. MDCTA has only several limitations. The detection threshold of the tiny arteries is lower than with CA and the opacification is static when compared to the dynamic aspect of CA which can better detect the direction of blood flow particularly in the collateral pathways. The fact that all arteries are opacified simultaneously can make spatial analysis difficult. Fortunately, secondary high quality selective reconstructions are able to dissociate and analyse the complexity of arterial superposition anatomic overlays. This nevertheless requires a good skill in the use of 3D post-processing programs.
MDCTA offers the opportunity to quickly diagnose or rule out mesenteric stenosis or compression in patients presenting with suggestive abdominal pain or angina. It also constitutes a primordial advance progress to plan the arterial safety of many major abdominal surgical procedures comprising classical aorto-iliac surgery, endovascular aneurysm repair (EVAR), complex pancreatic and gastrointestinal or colonic surgery but also to optimally plan revascularization of the mesenteric system through percutaneous angioplasty (PTA), stent placement or surgical bypass [1].
During embryogenesis, most segmental arteries regress and only three dominant major mesenteric visceral arteries persist: the celiac trunk (CTK), the superior mesenteric artery (SMA) and the inferior mesenteric artery (IMA) [1]. Fortunately, this mesenteric circulation has or may develop an extensive collateral network to ensure sufficient blood supply and in most cases these interconnections may easily supply if significant stenosis develops in one major artery.
Previous studies have suggested that a significant stenosis of at least two of the three main digestive arteries must occur and/or that a complete occlusion of the CTK must precede the occlusion of the rest of the mesenteric arteries before the occurrence of clinical symptoms of mesenteric angina [2]. Therefore, complaints related to symptomatic stenotic disease or chronic mesenteric ischemia which represents a serious and complex vascular disorder remains a rather rare event when compared with the high prevalence of chronic mesenteric atheromatous disease [1,3]. A stenosis of at least 70% in the mesenteric arteries may be considered as the cut-off for collateral development and increased compensatory blood flow [3].
This extensive pictorial review illustrates a large variety of situations which may be found during clinical practise. Single compression or stenosis of each digestive artery, combined and/or complex associations of stenosis and/or compressions of several arteries, secondary complications like aneurysms and classical but also sometimes unusual patterns of collateralizations are richly illustrated. Specific syndromes such as the median arcuate ligament syndrome (MALS) and the Leriche's syndrome that are also discussed.

Compression and stenosis of the celiac trunk (CTK)
The incidence of hemodynamically significant CTK stenosis in an asymptomatic population has been evaluated to 7.3% and the most important etiology is extrinsic compression by the median arcuate ligament (MAL) of the diaphragm. Atherosclerosis remains only a rather minor cause of stenosis of the CTK [4]. The MAL is a fibrous arch that connects the right and left diaphragmatic crura and defines the anterior margin of the aortic hiatus [5].
The Dunbar syndrome induced by the celiac trunk compression syndrome (CTCS) also called the median arcuate ligament syndrome (MALS) is a potential clinical entity characterized by a triad comprising epigastric pain, weight loss and postprandial pain with nausea and vomiting [5][6][7][8][9][10]. These symptoms are believed to be secondary to intermittent ischemia especially during the expiration phase [8]. These symptoms are attenuated when the patient is in an erect position and during inspiration [6,9]. Indeed, in these positions the CTK descends in the abdominal cavity and becomes more vertical resulting in a relief or attenuation of the compression [7,9,[11][12].
Atypical manifestations of the MALS are extremely variable ranging from exercise related pain and diarrhea in elite athletes to dramatic rupture of a secondary pancreaticoduodenal artery aneurysm (PDAA) developing on collaterals [5,8]. Nevertheless, the hypothesis that CTCS may lead or not to the clinical picture of MALS remains controversial [6,13]. Indeed nearly 13 to 50% of asymptomatic patients may exhibit a variable degree of compression during imaging. Thus, not only the compression but also the symptoms must then be simultaneously present to allow the diagnosis of MALS.
The physiopathology of MALS is also controversial: are the symptoms really caused by ischemia of the gut itself or by neurogenic compression or ischemia of the celiac ganglion [9]?
During MDCTA the MALS exhibits a characteristic hooked appearance of the focal narrowing of the CTK and the deformation increases during expiration (Figures 1 and 2). This aspect is clearly distinctive from other causes of stenosis such atherosclerosis [9]. Poststenotic dilatation of the compressed CTK is also common as well as the development of collaterals which essentially concern serpiginous hypertrophy of the Gastroduodenal Artery (GDA) and of the cephalic pancreatic arcades (CPAs) (Figures 1 and 3). These antero-inferior and postero-superior CPAs envelop the pancreas head in a circular network [14]. They anastomose the GDA originating from the hepatic artery (HA) with the inferior pancreaticoduodenal artery originating from the SMA usually as its first branch. It is our opinion that the presence of these collaterals is crucial for the diagnosis of a significant or high degree of compression of the CTK even if the deformation of the CTK is moderate. Indeed, most of the abdominal MDCT are performed in deep inspiration which classically reduces and thus underestimates the compression syndrome. The presence of collaterals helps to diagnose this underestimation. The principle should be: no collateralisation, no MALS except if an additional stenosis on the SMA is present compromising the development of collaterals. Nevertheless, the presence of these collaterals proves that the compression is significant but also demonstrates a good substitution.
As confirmed by several studies the CTCS of MALS is better appreciated during expiration (Figure 2) especially during dynamic duplex and color flow Doppler sonography that are considered by various authors as excellent diagnostic modalities to diagnose significant MALS and to distinguish it from a real atheromatous CTK stenosis in which respiratory variation are absent [7,9,[11][12]14].
Due to the permanent mechanical extrinsic compression experienced by the CTK in high-grade MALS only a short relief of symptoms followed by early restenosis is classically found after percutaneous angioplasty (PTA) with stenting. The traumatic effects of PTA on the intima and media may weaken the vessel which may become more susceptible to collapse. In addition, stent deployment may be compromised by slippage, mechanical fatigue or crushing secondary to permanent external compression (Figure 4). Therefore, the MALS may be considered as a relative contraindication of PTA or stenting and so compared with the thoracic outlet, the inguinal ligament and the popliteal space [8].
For the same reasons of chronic mechanical compression and major cyclic variation of flow during breathing the potential role of MAL in the development of CTK aneurysm and/or CTK dissection has also been reported (Figure 2) [5,15].

Double compression of the CTK and SMA by the MAL
Occasionally, in addition to the CTK the constricting effect of MAL may also manifest on the SMA and rarely on the renal arteries (RAs) [8][9][10]. If the compression on the SMA is important the development of the typical collaterals is compromised and the indirect and more distal substitution by of the IMA may be required (Figures 5,  6, 7, 8 and 9).       Corresponding angiographic images (f, g) confirm the high-grade stenosis of both vessels with post stenotic dilatation (red area on f). The stenosis of the SMA is first treated by a stent which unfortunately migrates more distally (black arrow). The interventional procedure is completed by single balloon dilatation of both arteries and a significant improvement of symptoms is obtained.
Nevertheless, this type of double compression has only been infrequently reported. Only four of the 51 patients with MAL syndrome reported by Reilly had both CTK and SMA compressions [16]. Other isolated cases have also been sporadically reported [12,[17][18][19].
A patient with a CCMT is potentially deprived of some of the protective benefits of dual origin vessels with multiple mutually supporting anastomoses. Occlusion or proximal stenosis affecting a common CCMT can have serious ischemic consequences to the intestine because the classical redundancy between the CA and SMA circulation is absent. Moreover, any disorder involving the common CCMT (dissection, thrombosis, emboly, atheromatosis) or an extensive surgery (for example a Wipple's procedure on the pancreas) may have dramatic consequences on the major abdominal viscera [20,22].

Secondary aneurysms
Stenosis, occlusion and compression of the CTK by the MAL is known to be one of the main factors for increased collateral circulation and secondarily also to the formation of about 50 to 60% of all pancreatico artery aneurysms (PDAAs) [5,[23][24][25].
When compression occurs on the CTK compressed by MAL during expiration the CTK territory becomes abruptly supplied by reverse flow from the SMA through the PDAs causing acute hemodynamic stress in these arteries and promoting aneurysmal formation (Figures 9 and 13) [5,[25][26]. These hemodynamic changes may affect the wall shear stress (WSS) of the arteries and a close relationship between a high WSS and the initiation of aneurysm formation has already been demonstrated in animal models [23][24]. PDAAs have also been demonstrated in case of AMS stenosis (Figure 4). Authors [25][26][27] have reported that aneurysm size did not correlate with rupture and suggest that PDAAs should then be treated at the time of diagnosis. The rupture of these aneurysms is a life-threatening emergency (Figure 14).

Collateral pathways between the SMA and AMI
The IMA is the smallest of the three main mesenteric arteries and supplies the distal transverse, descending and sigmoid colonic segments as well as the rectum [28]. It receives collaterals from the lumbar arteries, the median sacral artery and internal iliac arteries but also has primordial anatomic communications with the SMA. Vascular and abdominal surgeons are aware of this important collateral pathway between the IMA and the SMA. Indeed, inadvertent ligation or section of this important collateral network during aortic or abdominal surgery and especially in the presence of under-diagnosed stenosis of the SMA may have disastrous consequences, especially on the small intestine and left colon [29][30]. The collateral pathway between the SMA and the AMI is not always clearly designed. There is a real lack of consensus in the terminology used in the literature causing much confusion. Many denominations are used comprising the arch of Riolan (AR) (considered as a vague historic term to discard) (Figures 16 and 17), the meandering mesenteric artery (MeA) of Moskovitch (actually considered as the more precise term), the central anastomotic artery, the mesomesenteric artery, the middle left colic artery, the anastomosis of Riolan, the meandering artery or the great colic artery of Riolan but also the arch of Treves, the artery of Moskovitch, the anastomosis of Haller and many other names [29][30].
A pragmatic description consists to delineate three concentric different pathways running from the central mesenteric root to its periphery along the colon and comprising: • Centrally, the inconstant arch of Riolan (AR), joining the middle and left colonic artery and running very close to the inferior mesenteric vein. • In an intermediate location, the mesentery, the pathway observed in cases of severe stenosis or occlusion of the SMA and known as the Meandering Artery (MeA) (Figures 3, 4, 6, 7, 11, 12, 13 and 18). • Finally, in the extreme periphery of the mesentery, the marginal arcade of Drummond (MAD), which is classically not tortuous and runs along the left descending colon [28] (Figures 3 and 17).   Figure 10 continued (d, e, f, g). Major suppleance of the stenotic CCMT CTMC is assumed by a large MeA (black arrows). Nevertheless, the emergence of the feeding IMA (green circle) also appears critical. This artery emerges just above the distal thombotic segment of the aorta, appears atheromatous with significant stenosis and also appears somewhat wedged between the aorta and the synthetic aorto-iliac bypass.

c). Global VR view (a) shows massive collateralizations comprising hypertrophied anastomoses between the EAs (white arrowheads) and the ITAs (black arrowheads) and recruitment of the deep circumflex iliac arteries (grey arrowheads). Massive contribution of the digestives arteries is also present with anastomoses between the hypertrophied IMA (black arrow) and the IIAs via the inferior and medial
ReAs (green area on Figure 12a). The emergence of the hypertrophied IMA was nevertheless compromised by the aortic thrombosis (blue arrow). The consequence was the feeding of this hypertrophic IMA by a large MeA (white arrows) developing as a large sinuous anatomose between the IMA and the SMA. Moreover, the SMA had a common aortic emergence with the CA creating a rare but typical CCMT (within the red circle). This variant probably explains the absence of hypertrophied PDAs.    network (b, c) shows CTK (white arrowhead) and SMA (black arrowhead) of very good calibre. Nevertheless, the arterial supply of the left and sigmoid colon appears very precarious (white star). The IMA (red arrow) and its branches have a very thin calibre and will be invariably compromised by the EVAR. Collaterals are poor essentially coming proximally from an atypical serpiginous collateral (white arrows) from the GDA (yellow arrowhead) and distally from rectal collaterals from the left IIA (black arrow). The risk of secondary ischemic colitis or necrosis was substantial but was judged inferior to the risk of spontaneous rupture of the aneurysm. The patient was successfully treated by EVAR.   views (a, b) of the abdominal vessels reveal an extremely severe atheromatous calcified stenosis of the CTK (blue arrow) and of the SMA (red arrow). A well-structured AR is present (white arrows). It is centrally located and well distinct from the peripheral MAD (yellow arrow). This cartography allows the planning of an optimal surgical treatment (c). A long transmesenteric saphenous-vein bypass graft was performed with an implantation of the lower aorta (yellow arrowhead), a laterolateral anastomose with the SMA (white arrowhead) and a terminal lateral distal anastomose with the HA (green arrowhead).
Many authors consider that the anatomic AR and the MeA of Moskowitz are the same entity, the MeA being the term classically describing the tortuous hypertrophic expansion of the AR in the presence of stenosis or obstruction of the SMA or of the IMA. The expansion of the MeA is greater in presence of stenosis or occlusion of the SMA or in the presence of combined stenosis of SMA and CTK than in isolated stenosis of the IMA because the blood flow load is greater for the SMA than for the IMA [31].
In the presence of a large MeA it is thus recommended to surgeons to abandon or to seriously reconsider their plan for a major resection of the left colon [29]. Secondary necrosis of the right colon and entire small intestine may indeed produce if the flow is reverse in the MeA and necrosis of the sigmoid colon and upper rectum may produce if the flow is antegrade (Figure 3).

Aorto iliac occlusive disease (AIOD)
AIOD is most frequently a progressive chronic disease resulting of massive deposition of atheromatosis at the level of the aortic bifurcation and on the segment of aorta proximal from this bifurcation. Infrequent causes of AIOD are acute occlusion due to embolus or occlusion related to vasculitis [32]. Nevertheless, many patients remain underdiagnosed because they are asymptomatic as a result of the progressive development of massive rich collateral pathways.
The clinical Leriche's syndrome (LS) includes the typical triad of symptoms of claudication, impotence and decreased peripheral pulses [33]. In these patients MDCTA cartography is clinically critical for surgical planning and to avoid morbidity of inadvertent surgical injury (Figures  12, 18, 20 and 21) [32].
The VV pathways (deriving from embryologic segments of the ventral aorta) is provided by the CTK, SMA and IMA. This collateral pathway in which the digestives arteries are implicated becomes more prevalent in cases of AIOD extending more proximally along the aorta and thus approaching the level of the emergence of the RAs [32,34].   The SS collateral pathway (deriving from embryologic segments of the dorsal aorta) comprise subcostal, intercostal and lumbar arteries representing the afferent vessels (Figures 12 and 18). They can reconstitute and replace the external iliac arteries (EIAs) through anastomoses with the deep and superficial circumflex arteries or supply the internal iliac arteries (IIAs) through anastomosis with the superior gluteal artery and with the ilio-lumbar artery. Another SS collateral system is provided by the sacral plexus where the lateral sacral arteries coming from the IIA and the median sacral artery coming from the aorta just above the aortic bifurcation develop collaterals [34].
The internal thoracic artery (ITA) (also called internal mammary artery), and the superior and inferior epigastric arteries (EA) also constitute another SS collateral pathway of primordial importance for the lower limbs (Figures 12  and 18). Inadvertent injury to this parietal vertical system indirectly anastomosing the subclavian arteries with the EIAs -for example during abdominal surgery or because of inadequate recruitment of the ITAs for coronary bypass -may because acute ischemia in the lower limbs [34][35]. Moreover, the inappropriate suppression of this parietal pathway may also intensify the contribution of the visceral arteries (the VS pathway) to supply the lower limbs and initiate chronic mesenteric ischemia or mesenteric claudication.
Finally, the VV pathway is also constituted by a cross pelvic collateral system constituted by communication between the superior, middle and inferior rectal arteries (ReAs) on both sides (Figures 12 and 18).
In each patient presenting with AIOD, the final collateral pattern is individually constituted by a mix of all these above described pathways. It essentially depends of the level of the occlusion: above the IMA, at the level of the IMA or below the IMA. The most proximally the aorta is occluded -from the iliac bifurcation (or under) to just under the level of emergence of the renal arteries -the most important is the recruitment of the digestive arteries and collateralization successively implicates the IMA, the SMA and finally the CTK itself [34]. An optimal cartography of the different possible collateral pathways is thus also necessary to predict the capabilities of the patient to tolerate inadvertent or intentional ligation or embolization of pelvic arteries or pelvic surgery such as left colonic or sigmoid resection (Figure 15).

The falciform artery (FA)
The FA is a branch of the hepatic artery (HA) that develops anastomoses with the vertical pathway constituted by the EA and the ITA. The FA may thus constitute a VS collateral pathway (in case of Leriche syndrome -LS) or a SV collateral pathway (in case of stenosis of the digestive arteries).  Figure 19 continued. Multiple selective 3D VR reconstructions (f, g, j, k) and MIP view (h) illustrate huge tortuous collateral arterial network comprising hypertrophied anastomoses between the EAs (white arrowheads) and the ITAs (yellow arrowheads) especially on the right side. Additional collateralisation had developed in the right upper quadrant through recruitment of the HA artery via a large FA (red circle and red arrow). Massive collateralization had also developed in the pelvic area (blue circle) where huge tortuous collaterals coming from the hypertrophied IMA (green arrow) are developing anastomoses with the IIA on the right and with a huge tortuous obturatrice artery (orange arrow) supplying the superficial femoral artery on the left. The emergence of the hypertrophic IMA (green arrow) is occluded by the aortic thrombosis but is supplied by a huge IMT or AoR (purple arrow) coming from the SMA (blue arrow). The episodes of left colonic ischemia are attributed to a steal syndrome from the left leg. Symptoms were successfully healed through a Hartmann procedure comprising segmental colonic resection and left colostomy.
The FA is essentially known by interventional radiologists who perform selective hepatic angiography [13]. They are aware of the potential supraumbilical skin complications which may be produced by inadvertent distribution of chemotherapeutic agents through this artery when they perform transcatheter chemoinfusion or chemoembolization for liver tumours. Otherwise the spontaneous visualization of the HFA is very uncommon in current abdominal CT practice [13].
To our knowledge, there are no studies reporting the prevalence of the FA detection during dynamic CT studies in healthy patients. Nevertheless, our opinion, based on our personal experience with 64-row multidetector CT is that this prevalence remains extremely low [13].
In a previous report, we reported two cases in which it was likely that the FA was visualized because it was enlarged by a compensatory phenomenon related to the critical state of digestive arteries of the patients. One had a CCMT and the other had severe compression of the CTK and of the SMA by the MAL [13]. Additional cases are illustrated in this pictorial review and were found in cases of LS (Figure 21) or in cases of compression of the CTK by the MAL (Figures 6 and 19).

Other unusual collateral pathways
Left and right inferior phrenic arteries (IPAs) are other rare arteries being able of collateralization with the HA or with the CTK (Figure 19). As for the HFA, these arteries are also known by interventional radiologist as potential extrahepatic collateral arteries [36]. They may supply hepatic adenocarcinoma or act as collaterals in patient presenting with stenosis of the CTK (Figures 4 and 10). Unusual extrahepatic collaterals may also concern accessory RAs ( Figure 6).
In our experience, we also recently found two cases of atheromatous stenosis of the splenic artery (SA) fortuitously diagnosed through the presence of unusual collateralisation. The first case was collateralized by a tortuous gastroepiploic artery (GEA) a situation which has only exceptionally been described in rare cases of absence or occlusion of the SA [37] (Figure 22). The other case was supplied by an enormous meandering hypertrophy of the arcus epiploica magnus of Barkow. To our knowledge this last type of collateralisation has never been described before (Figure 22).

Conclusion
Through this extensive pictorial review, we have illustrated a large diversity of complex abdominal situations implicating the digestive arteries and/or the systemic abdominal arteries, the two arterial systems being frequently interconnected. These situations are not uncommon in clinical practise. We confirm and demonstrate that multidetector computed tomographic angiography (MDCTA) can be very effective not only to diagnose a single arterial stenosis or compression but also to dissect combined and/or complex associations of multiple stenosis and/or compressions of several arteries. MDCTA also appears uncompetitive unavoidable to map sometimes very complex networks of collateralization.  (a, b). The arterial supply of the spleen is preserved through an important collateralization by the hypertrophied main GEA (black arrows) a branch of the GDA (red arrow). In this 58-year-old patient (c, d) an extremely rare collateralization of a stenosed atheromatous SA (white arrow) is constituted by a huge meandering hypertrophy of the omental arterial arcade of Barkow (yellow arrowhead). This arcade is also feed by the GDA (red arrow).
MDCTA is confirmed being the gold standard for the diagnostic evaluation of abdominal and/or mesenteric arterial diseases. It represents a primordial advance to plan the safety of the digestive vascularisation before many major abdominal surgical procedures and to plan revascularization of the mesenteric arterial system itself.