Collateral circulation develops in stenosis of the celiac trunk and superior mesenteric artery

Mesenteric circulation is provided by the celiac trunk (CT), superior mesenteric artery (SMA), and inferior mesenteric artery (IMA). The collateral circulation between CT and SMA and between SMA and IMA plays a protective role against intestinal ischemia in case of narrowing or occlusion of the mesenteric vessels. In our study, it is aimed to determine the CT and SMA stenosis rates in patients with CT and SMA stenosis from angiography images, the occurrence of the collateral variations, and the frequency of these variations. A total of 408 non-selective or selective CT and SMA angiographic images were taken of 215 patients (130 males, 85 females) who were admitted to Akdeniz University Hospital with symptoms of chronic mesenteric ischemia (CMI) were included. The angiography images were analyzed in regards to CT and SMA stenosis rates, and the collateral variations between mesenteric vessels. Stenosis of CT was observed in 14 patients, whereas the stenosis of the SMA was observed in 12 patients. The most common collateral vessel in these patients was the gastroduodenal artery. Both stenoses of CT and SMA were found in 9 patients. The Riolan arch was the most common type of collateral vessel in these patients. It was observed that mesenteric circulation was mainly provided by gastroduodenal artery in patients with isolated CT or SMA stenosis or occlusion while in patients with stenosis or occlusion of both CT and SMA, mesenteric circulation was mainly provided by the Riolan arch. A significant increase was observed in the prominence of collateral vessels in patients with stenosis of more than 70%.


Introduction
Mesenteric blood flow is supplied by the celiac trunk (CT), superior mesenteric artery (SMA), and inferior mesenteric artery (IMA). Anatomic variations of these arteries, which are responsible for the blood supply of the abdominal regions, have been commonly reported as clinically importance in these arteries. In a cadaveric study, Cicekcibasi et al., found a coeliacomesenteric trunk that gives rise to the left gastric, the common hepatic, the splenic, the left gastro-epiploic, and the right and left inferior phrenic arteries in 62-year-old male cadaver [5]. In the study evaluating both proper hepatic artery and gastroduodenal artery (GDA) variations on multi-detector computed tomography angiography (MDCT) of 671 patients, Ekingen et al. found 35 different types related to PHA and GDA. The authors reported different anatomical variations in 300 of 671 patients [7]. In another study evaluating the variation of CT, SMA, and hepatic artery in 607 patients on MDCT, they found that the most common type of variation was found to be the origin of the right hepatic artery from SMA (9.6%), and the next most common variation was the origin of the left hepatic artery from the left gastric artery (6.9%) [8]. Chronic stenosis or occlusion in these vessels can be compensated for by collateral vessels connecting these vessels to each other [2,12,17,28,30,35]. Symptoms are typically indistinct until obstruction of at least two mesenteric vessels. Collateral circulation has a protective role against intestinal ischemia when there is obstruction of mesenteric vessels [13,30]. In cases of stenosis of mesenteric vessels, the existing collateral vessels expand as a response to arterial hypotension in the distal of the obstruction [13,30,33,34,36].
The main collateral circulation between the CT and SMA is provided through the GDA and dorsal pancreatic artery (DPA) [11,30,33,34]. The Bühler arch of embryological origin, another arterial connection, is an uncommon and rarely reported vessel that provides a direct connection between the CT and SMA [4]. This arch represents a remnant of anastomosis between the 10th and 13th ventral segmental arteries embryologically [31]. There is no connection between the Bühler arch and with the GDA and DPA. When the GDA or DPA remains insufficient in mesenteric stenosis, the Bühler arch can provide an additional connecting route, and therefore, its presence is important [21]. There are two important collateral circulation pathways between the SMA and IMA [32]. In this way, normal blood circulation passes to the transverse colon and descending colon from the Drummond marginal artery [19,29,35]. The Riolan arch, which is more centrally located within the mesenterium, is another important connection between the SMA and IMA when there is arterial occlusion or stenosis. In proximal SMA occlusion, the Riolan arch provides collateral flow that may be retrograde [20,23].
Although stenosis of the mesenteric arteries is commonly seen, ischemic complaints develop in very few patients. The development of ischemic complaints associated with stenosis in a single mesenteric artery can be prevented by collateral circulation [26,30,35]. Detailed knowledge of the presence and frequency of collateral vessels before a surgical procedure is crucial in surgical interventions to be applied to the abdominal region and is an important factor for the success of the operation [9]. The aim of this study was to determine the degree of CT and SMA stenosis on the angiography images of patients with CT or SMA stenosis, and to examine the presence and frequency of collateral variations.

Materials and methods
The present study was approved by the Clinical Research Ethics Committee of Akdeniz University (decision no: 212, dated: 28/04/2021). A retrospective evaluation was performed of the angiography images of 215 patients referred to Akdeniz University Medical Faculty with an initial diagnosis of chronic mesenteric ischemia. The patients comprised 130 males and 85 females with a mean age of 62 years (18-93 years). The vessels observed to be narrow on the angiography images were classified according to stenosis degree of < 50%, 51-70%, 71-99%, and occlusion by two interventional radiologists with 8 and 23 years of experience (Fig. 1).
The angiography examinations were performed using a Toshiba Infiniks 8000 C, DSA device (Toshiba Medical Systems Corporation, Japan) in the Radiology Department. Non-selective abdominal aorta arteriography was performed on all the patients, then selective images were obtained as required. In the non-selective angiographic procedures, a multi-hole pigtail catheter was used (Cordis Corporation Angiographic Catheter, A Cardinal Health Company USA). In the acquisition of the selective CT, SMA, and other selective images, a renal double curve catheter (RDC Angiographic Catheter, Cordis Corporation, A Cardinal Health Company USA), a Simmons type 1, and Simmons type 2 catheter (Sim 1,2 Angiographic Catheter, Cordis corporation, A Cardinal Health Company USA) were used.

Results
Stenosis on angiography of the CT and SMA was found in 35 patients. Stenosis in the CT was observed in 14 patients, in the SMA in 12 patients, and in both the CT and SMA in 9 patients. The mesenteric arteries with stenosis and the degree of the stenosis according to gender are presented in Table 1. Collateral vessels observed between the CT and SMA are presented in Figs. 2 and 3, and collateral vessels observed between the SMA and IMA are presented in Figs. 4 and 5.
The mesenteric arteries with stenosis on the angiographs and collateral vessels according to the degree of the stenosis are presented in Table 2. It was observed that collateral circulation was provided by the GDA in 2 of the 10 patients with CT stenosis < 70%. It was observed that collateral circulation was supplied by the GDA in 2 patients and by the Riolan arch in one patient with 71-99% CT stenosis. In one patient with occluded CT, collateral circulation was provided by the GDA. In female patients with CT stenosis, collateral circulation was found to be mainly provided by the GDA. In the 5 male patients with CT stenosis, the stenosis degree was < 70% and any collateral vessel was not seen in these patients.
Of the 3 male patients with < 70% SMA stenosis, DPA was determined in one patient, and Drummond marginal artery in one patient. Collateral vessels were found in all 6 patients with < 70% stenosis. Of the female patients, GDA was determined in one patient, and both GDA and Riolan arch in the other patient. In one female patient with stenosis of 90% and a history of angioplasty, GDA, Riolan arch, and Drummond marginal artery were observed. Of the male patients, Riolan arch and Drummond marginal artery were determined in one patient, GDA and Riolan arch in one patient, and PDA and Drummond marginal artery in one 1 3 patient. Occluded SMA was determined in one female and 2 male patients. GDA, Bühler arch, Riolan arch, and Drummond marginal artery were found in the female patient. Of the 2 male patients, GDA and Riolan arch were determined in one patient, and only GDA in the other patient. In the patients with only SMA stenosis, it was observed that collateral circulation was provided by GDA in female patients whereas by the Riolan arch in male patients.
Of the 3 patients with < 70% stenosis in both the CT and SMA, the Riolan arch was determined in one female patient. In one female patient with SMA occlusion and < 70% CT stenosis, Riolan arch was determined. In another female patient with occluded SMA and > 70% CT stenosis, GDA, DPA, and Riolan arch were determined. Riolan arch was observed to be present in all 4 patients with occlusion of both the CT and SMA. In addition, Drummond marginal artery was determined in 2 female patients and GDA in one male patient.

Discussion
The gastrointestinal system has extensive and complex arterial circulation, which provides a sufficient blood supply for the digestive process and plays a protective role against intestinal ischemia in case of narrowing or occlusion of the mesenteric vessels [1,6]. Detailed knowledge of the collateral vessels which can occurred between the CT and SMA or  between the SMA and IMA is important for the appropriate evaluation and management of the various disease processes that may affect the vascular supply of the gastrointestinal system. Therefore, several studies have been conducted on mesenteric collateral circulation between these vessels [11,21,30,33,34].
In their study, in which the angiography images of 94 patients with CT stenosis were evaluated, Song et al., reported that the presence of GDA was determined in 77 and PDA in 61 of 81 patients with normal hepatic artery anatomy. Of the 13 patients with variant hepatic artery, GDA was reported to be present in 12, and PDA in 10 [30]. In our study, of the 14 patients with isolated CT stenosis, GDA was observed in 5 patients and the Riolan arch in one patient. The absence of collateral vessels in male patients with CT stenosis may be due to a stenosis degree of less than 70% in male patients.
When the GDA or PDA is insufficient in collateral circulation, the Bühler arch provides an additional collateral pathway and is important in the alleviation of ischemia-related symptoms [21,27]. Due to the difficulties in the determination of the Bühler arch, there are only a few studies in the literature related to the Bühler arch. The prevalence of the Bühler arch in studies performed on different populations has been reported to be a mean of 1.71% (range 0.3-4.1%) [21]. Saad et al. examined the angiography images of 120 asymptomatic liver donors and determined Bühler arch in 4 cases [27]. In another study, Ferrari et al. examined the MDCT images of 60 asymptomatic patients and reported Bühler arch in 2 cases [9]. Similarly, Ognjanovic et al. determined the presence of the Bühler arch on 5 of 150 MDCT images of asymptomatic patients [24]. In another study, in one case, an abnormally dilated and tortuous Bühler arch in the absence of CT stenosis reported in one case [25]. In our study, we observed the Bühler arch in one patient (0.46%) of 215 angiography images, and our finding was consistent with the current literature. Although the Bühler arch is a rare anatomical variation, the presence of this arch is important for embryology, general surgery, and interventional radiology. It may also provide information about the developmental processes defining adult anatomy [21]. The presence of the Bühler arch should also be taken into consideration during surgical interventions in this region such as pancreaticoduodenectomy [14,21,25].
The Riolan arch and the Drummond marginal artery are important connections providing collateral blood flow between the SMA and the IMA in when the presence of an    1 3 in 9 cases, descending colon-sigmoid colon cancer in 8 cases, active ulcerative colitis in 5 cases, and severe IMA stenosis in 2 cases [36]. Normally, as the blood flow load of the SMA is higher than that of the IMA, it has been reported that the Riolan arch expands more in patients with SMA obstruction or severe stenosis than in patients with IMA occlusion [36]. In our study group, the most common collateral vessel in patients with isolated SMA stenosis was the Riolan arch. The presence of the Riolan arch in all patients with both CT and SMA occlusion suggests that collateral circulation is mainly provided through the Riolan arch in these patients. In a study by van Petersen et al., 228 patients with suspected chronic mesenteric ischemia were examined, and of 65 patients found to have CT and SMA stenosis of < 70%, GDA was determined in 7 patients, Bühler arch in one patient, and Riolan arch/Drummond marginal artery in 10 patients [34]. Of the cases observed to have < 70% CT stenosis and > 70% SMA stenosis, GDA was determined in 2 cases, and Riolan arch/Drummond marginal artery in 3 cases. Of the 21 patients found to have > 70% CT and SMA stenosis, Riolan arch/Drummond marginal artery was determined in 15 patients. van Petersen et al., stated that collateral blood flow was basically provided through the GDA only in patients with CT stenosis [34]. Similar to the findings of van Petersen et al., the most common collateral vessel in patients with isolated CT stenosis in our study was the GDA, supporting the view that the GDA has an important role in mesenteric blood circulation in patients with isolated CT stenosis. Consistent with the findings of van Petersen et al., the Riolan arch was determined to be the most common collateral vascular pathway in patients with both CT and SMA stenosis in the present study [34]. This finding supports the view that the Riolan arch provides important collateral blood flow between the proximal SMA and IMA when stenosis is present in the CT and SMA. Therefore, this collateral vessel is extremely important for vascular and gastrointestinal surgeons during operative procedures.
van Petersen et al. reported that mesenteric stenosis > 70% leads to more collateral development and higher flow velocities in the non-stenotic vessel [34]. In our study, similar to the findings of van Petersen et al., the vast majority of collateral variations were observed in patients with > 70% stenosis. This finding suggests that the rate of 70% stenosis in mesenteric vessels could be a threshold value for collateral development and increasing collateral blood flow. The higher rate of collaterals in females with CT stenosis than males could be due to the fact of the male cases having stenosis < 70%.
Collateral variations related to CT and SMA stenosis and the frequencies of these variations were investigated in this study. The limitation of this study was the inclusion of the small number of included patients with an initial diagnosis of mesenteric ischemia. There is, therefore, a need for further studies including a greater number of cases to be able to comprehensive evaluation of collateral development in patients with stenosis.
As arterial vascularization of the gastrointestinal system is mainly supplied by CT, SMA, and IMA, anatomical variations or anomalies of these vessels and their branches have also been frequently reported [3,12,18,22]. Iezzi et al. have examined the anatomy and normal variants of CT on 555 MDCT angiographies and detected the hepato-splenic trunk, hepato-gastro-splenic trunk, and the gastro-splenic trunk in 50.4, 19.4, and 2.3% of the cases, respectively [12]. In a study using angiography computed tomography study, Mrowiec et al., reported the absence of CT and connections of left gastric artery, splenic artery, and common hepatic arteries with origin above the SMA in patients undergoing radical pancreaticoduodenectomy [22]. In another study, replacement of the right hepatic artery and common hepatic arteries to the SMA was seen in a patient with hepatocellular carcinoma [3]. In a systematic review of splenic artery variations, Manatakis et al. reported that the splenic artery originated from the CT in the vast majority of specimens (97%), but it also originated from the abdominal aorta (2.1%), and SMA or the common hepatic artery (0.7%) [18]. The awareness of both anatomic variations of major abdominal vessels and the presence of collateral vessels occurring in case of CT and SMA stenosis enhances the knowledge of that region. To avoid intraoperative vascular injury major postoperative complications, it is an essential to knowledge of major abdominal vessels and collateral variations which provides connections between these vessels.

Conclusion
The results of this study indicated that GDA was the most common collateral vessel both in patients with isolated CT stenosis and those with isolated SMA stenosis, and this finding suggests that a large proportion of mesenteric blood flow in these patients is provided through the GDA. That the Riolan arch was detected in all the patients with both CT and SMA occlusion showed that collateral blood flow in these patients was mainly provided by the Riolan arch. Detailed knowledge of the collateral vessels related to stenosis in CT or SMA is essential for the prognostic assessment of acute and chronic ischemia, as well as for the planning and safely performing of surgical approaches, such as pancreatico-biliary, colon surgery, and liver transplantation. A significant increase was determined in the presence and number of collateral vessels in patients with > 70% stenosis. Therefore, the determination of collateral vessels in preoperative angiographic images before surgical intervention is performed in the abdominal region is of critical importance