Collateral Circulation Develops in Stenosis of the Celiac Trunk, and Superior Mesenteric Artery

doi:10.21203/rs.3.rs-2226314/v1

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Collateral Circulation Develops in Stenosis of the Celiac Trunk, and Superior Mesenteric Artery

https://doi.org/10.21203/rs.3.rs-2226314/v1

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published 13 Feb, 2023

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Purpose

Mesenteric circulation is provided by the celiac artery (CA), superior mesenteric artery (SMA), and inferior mesenteric artery (IMA). The collateral circulation between CA 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 CA and SMA stenosis rates in patients with CA and SMA stenosis from angiography images, the occurrence of the collateral variations, and the frequency of these variations.

Methods

A total of 408 nonselective or selective CA 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. Angiography images were analyzed in regards to CA and SMA stenosis rates, and the collateral variations between mesenteric vessels.

Results

Stenosis of CA 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 CA and SMA were found in 9 patients. The Rioalan arch was the most common type of collateral vessel in these patients.

Conclusion

It was observed that mesenteric circulation was mainly provided by gastroduodenal in patients with isolated CA or SMA stenosis or occlusion while in patients with stenosis or occlusion of both CA and SMA, mesenteric circulation was mainly provided by the Riolan arc. A significant increase was observed in the prominence of collateral vessels in patients with stenosis of more than 70%.

Mesenteric ischemia

Mesenteric collateral circulation

Celiac artery

Superior mesenteric artery

Mesenteric blood flow is supplied by the celiac artery (CA), superior mesenteric artery (SMA), and inferior mesenteric artery (IMA). Chronic stenosis or occlusion in these vessels can be compensated for by collateral vessels connecting these vessels to each other [17, 21]. Symptoms are typically indistinct until obstruction of at least two mesenteric vessels. Collateral circulation takes on a protective role against intestinal ischaemia when there is obstruction of mesenteric vessels [17]. In cases of stenosis of mesenteric vessels, the existing collateral vessels expand as a response to arterial hypotension in the distal of the obstruction [17, 20–22].

Main collateral circulation between the CA and SMA is provided through the gastroduodenal artery (GDA) and dorsal pancreatic artery (DPA) [5, 17, 19, 20]. Bühler arch of embryological origin, another arterial connection, is a not common and rarely reported vessel that provides a direct connection between the CA and SMA [1]. This arch represents a remnant of anastomosis between the 10th and 13th ventral segmental arteries embryologically [18]. There is no connection between the arch of the Bühler with the GDA and DPA. When the GDA or DPA remain insufficient in mesenteric stenosis, the Bühler arch can provide an additional connecting route, and therefore, its presence is important [12]. There are two important collateral circulation pathways between the SMA and IMA. In this way, normal blood circulation to the transverse colon and descending colon from the Drummond marginal artery [16, 21]. 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 [11].

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 [14, 17, 21]. 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 [3]. The aim of this study was to determine the degree of CA and SMA stenosis on the angiography images of patients with CA or SMA stenosis, and to examine the presence and frequency of collateral variations.

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.

The angiography examinations were performed by 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 CA, 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.

Stenosis on angiography of the CA and SMA was found in 35 patients. Stenosis in the CA was observed in 14 patients, in the SMA in 12 patients, and in both the CA 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 CA and SMA are presented in Fig. 1, and collateral vessels observed between SMA and IMA are presented in Fig. 2.

Table 1

The mesenteric arteries with stenosis and the degree of the stenosis according to gender
Vessels with stenosis	Stenosis rates	Female	Male
CA	< 70%	5	5
	> 71–99%	3	-
	Occluded	1	-
	Total	9	5
SMA	< 70%	-	3
	71–99%	3	3
	Occluded	1	2
	Total	4	8
Both CA and SMA	CA and SMA < 70%	2	1
	CA < 70%, SMA occluded	1	-
	CA > 70%, SMA occluded	1	-
	CA and SMA occluded	3	1
	Total	7	2
CA; Celiac artery, SMA; Superior mesenteric artery

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 CA 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% CA stenosis. In one patient with occluded CA, collateral circulation was provided by the GDA. In female patients with CA stenosis, collateral circulation was found to be mainly provided by the GDA. In the 5 male patients with CA stenosis, the stenosis degree was < 70% and any collateral vessel was not seen in these patients.

Table 2

Mesenteric arteries with stenosis on the angiographs and the collateral vessels according to the stenosis degree.
Vessels with stenosis	Stenosis rates	GDA	DPA	R	D
CA	< 70%	2	-	-	-
	> 71–99%	2	-	1	-
	Occluded	1	-	-	-
	Total	5	-	1	-
SMA	< 70%	-	1	-	1
	71–99%	4	2	4	3
	Occluded	3	1	2
	Total	7	4	6	4
CA and SMA both	CA and SMA < 70%	-	-	1	-
	CA < 70%, SMA occluded	-	-	1	-
	CA > 70%, SMA occluded	1	1	1	-
	CA ve SMA occluded	1	-	4	2
	Total	2	1	7	2
CA; Celiac artery, SMA; Superior mesenteric artery, GDA: Gastroduodenal artery, DPA: Dorsal pancreatic artery, R: Riolan arch, D; Drummond marginal artery

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 patient. Occluded SMA was determined in 1 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 Riolan arch in male patients.

Of the 3 patients with < 70% stenosis in both the CA and SMA, the Riolan arch was determined in one female patient. In 1 female patient with SMA occlusion and < 70% CA stenosis, Riolan arch was determined. In another female patient with occluded SMA and > 70% CA stenosis, GDA, DPA, and Riolan arch were determined. Riolan arch was observed to be present in all 4 patients with occlusion of both the CA and SMA. In addition, Drummond marginal artery was determined in 2 female patients and GDA in 1 male patient.

Although CA and SMA stenosis is a very common clinical condition, mesenteric ischemia rarely develops in patients with stenosis or occlusion in a single mesenteric artery. In patients with stenosis in the CA and SMA, the symptoms of mesenteric collateral circulation are reported to be reduced or delayed [2, 9].

It has been reported that in the majority of CA and/or SMA stenosis cases, anastomosis of the CA and SMA is formed by the GDA and PDA pathway [5, 12, 17, 19, 20]. 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 [12, 15]. Detailed knowledge of the collateral vessels associated with stenosis in CA or SMA is important for the prognostic evaluation of acute and chronic ischemia, as well as for the planning and more safely performing of medical procedures such as pancreaticobiliary and colon surgery, and liver transplantation [10, 17]. The presence of the Bühler arch should also be taken into consideration during surgical interventions in this region such as pancreaticoduodenectomy [6, 12].

In their study, in which the angiography images of 94 patients with CA 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 [17]. In our study, of the 14 patients with isolated CA stenosis, GDA was observed in 5 patients and the Riolan arch in one patient. The absence of collateral vessels in male patients with CA stenosis may be due to a stenosis degree of less than 70% in male patients.

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%) [12]. Saad et al. examined the angiography images of 120 asymptomatic liver donors and determined Bühler arch in 4 cases [15]. In another study, Ferrari et al. examined the multidetector computed tomography (MDCT) images of 60 asymptomatic patients and reported Bühler arch in 2 cases [3]. Similarly, Ognjanovic et al. determined the presence of the Bühler arch on 5 of 150 MDCT images of asymptomatic patients [13]. In our study, we observed the Bühler arch in one patient (0.46%) in 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 [12]. In surgical interventions applied to this region, the presence of the Bühler arch can cause intraoperative complications such as bleeding. Therefore, the potential presence of the Bühler arch should be taken into consideration during surgical and radiological interventions to the abdominal region.

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 occlusion or significant stenosis [4, 8]. There is usually a small amount and slow blood flow in the Riolan arch, which is recessive and of small diameter. It has been reported that the Riolan arch will generally expand after SMA obstruction and can therefore be fully visualized on angiography [4, 22]. As vascularisation of the descending colon is provided by the SMA, the Riolan arch is important in colorectal surgery, especially in cancer patients. In their study by Karatay et al., in which 115 abdominal CT images were evaluated, Drummond marginal artery was found in all the cases and the presence of Riolan arch was reported in 32 (27.8%) [7].

Xie et al. determined the presence of expanded Riolan arch in a total of 47 patients (29 males and 18 females) on MDCT images of 626 patients with large vessel lesions or intestinal disease. Of these cases with Riolan arch, severe SMA stenosis was determined in 16 cases, SMA obstruction in 9 cases, descending colon-sigmoid colon cancer in 8 cases, active ulcerative colitis in 5 cases, and severe IMA stenosis in 2 cases [22]. 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 [22]. 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 CA 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 CA 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 [20]. Of the cases observed to have < 70% CA 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% CA 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 CA stenosis [20]. Similar to the findings of Van Petersen et al., the most common collateral vessel in patients with isolated CA 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 CA stenosis. Consistent with the findings of Van Petersen et al., the Riolan arch was determined most common collateral vascular pathway in patients with both CA and SMA stenosis in the present study [20]. 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 CA 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 [20]. 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 CA stenosis than males could be due to the fact of the male cases having stenosis < 70%.

Collateral variations related to CA and SMA stenosis and the frequencies of these variations were investigated in this study. The limitation of this study was to include 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.

The results of this study indicated that GDA was the most common collateral vessel both in patients with isolated CA 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 CA 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 CA 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 pancreaticobiliary, colon surgery, and liver transplantation. The significant increase was determined in the presence and number of collateral vessels in patients with > 70% stenosis. Therefore, the determination of collaterals in preoperative angiographic images before surgical intervention is performed in the abdominal region is of critical importance for patient-specific surgical planning and for the surgical intervention to be performed safely.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the suitably constituted Ethical Committee at the Researches Department of University, within which the work was undertaken, and the study conforms to the Declaration of Helsinki.

Conflict of Interest

Authors declare that they have no conflict of interest.

Author Contributions

HS: project development, data analysis, manuscript writing. OO: data collection and data analysis. KE: data collection and data analysis. SO: data analysis, manuscript writing. MSD: manuscript writing, TS: project development, data analysis, manuscript editing, MS: project development, manuscript writing, manuscript editing. All authors read and approved the final manuscript.

Funding

The study had no funding source.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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published 13 Feb, 2023

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Collateral Circulation Develops in Stenosis of the Celiac Trunk, and Superior Mesenteric Artery

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