Open revascularization for chronic mesenteric ischemia in the endovascular era: a quaternary-center experience and management algorithm

Abstract Background Chronic mesenteric ischemia (CMI) is a debilitating disease with a heavy burden on quality of life. Stenting of the superior mesenteric artery (SMA) is the first option for treatment, but there is a lack of consensus defining precise indications for open revascularization (OR). Objectives To describe a series of 4 patients with CMI treated with OR and to present an algorithm for the management of this condition. Methods Three patients presented with typical intestinal angina and weight loss. One patient was subjected to prophylactic revascularization during open abdominal aortic aneurysm repair. Surgical techniques included: 1) Bypass from the infrarenal aorta to the SMA; 2) Bypass from an aorto-bifemoral polyester graft to the SMA; 3) Bypass from the right iliac artery to the SMA; 4) Bypass from the right graft limb of an aorto-biiliac polyester graft to the median colic artery at Riolan’s arcade. PTFE was used in all surgeries. All grafts were placed in a retrograde configuration, tunneled under the left renal vein, making a smooth C-loop. A treatment algorithm was constructed based on the institution’s experience and a review of recent literature. Results All patients demonstrated resolution of symptoms and recovery of body weight. All grafts are patent after mean follow-up of two years. Conclusions Open revascularization using the C-loop configuration is a valuable technique for CMI and may be considered in selected cases. The algorithm constructed may help decision planning in other quaternary centers.


INTRODUCTION
Chronic mesenteric ischemia (CMI) is a debilitating disease with a heavy burden on the quality of life of affected patients. 1There is also a risk of transformation into acute mesenteric ischemia, which is a catastrophic situation with a high mortality rate if not immediately treated. 1,2][5][6] The aim of this study is to describe a series of 4 patients with CMI who were treated with open revascularization and to present an algorithm for optimal management of this condition.

METHODS
This study was approved by the Ethics Committee of the Institution.(CAAE 61365322.8.0000.5404,Consolidated Opinion: 5.700.372).All patients signed an informed consent form.This is a retrospective, multicenter series of 4 consecutive cases (2 men, 2 women, mean age= 62.3 years, range 60-68 years) operated from February 2017 to February 2018 at 2 teaching hospitals in Brazil.Three patients presented with typical intestinal angina with significant weight loss in a relatively short period of time.One patient was operated for an abdominal aortic aneurysm and presented obstruction of the superior mesenteric artery and celiac trunk; she underwent prophylactic revascularization.One patient had undergone a previous unsuccessful superior mesenteric artery angioplasty.The patients' characteristics are shown in Table 1.
The patients' symptoms and anatomic findings are summarized in Table 2.
All operations were performed through a median laparotomy with general anesthesia and the patient in supine position.All procedures were headed by an experienced vascular surgeon assisted by 3 vascular surgery residents (4 years into specialized training).All grafts were placed in a retrograde configuration, tunneled under the left renal vein and caudal to the mesocolon mesentery, making a smooth C-loop, and were anastomosed using a polypropylene continuous suture to the superior mesenteric artery in an antegrade configuration, and in one case to the median colic artery, as previously described. 7 Systemic heparinization with 5000 IU of non-fractioned heparin was performed systematically 5 minutes before arterial clamping.Detailed surgical procedures are shown in Table 3.
The follow-up protocol included serial duplex ultrasound (DUS) performed by experienced radiologists at regular intervals after the procedure (at 1 month, at 1 year, and then annually).Computed tomography angiography (CTA) was performed if the US failed to assess the graft anastomosis.Figures 1 to 3 illustrate the preoperative CTA, surgical procedures, and postoperative imaging exams of some cases.

RESULTS
There were no deaths or complications in this series.All patients presented with complete resolution of the ischemic symptoms, body weight recovery, and a patent graft.Postoperatively, patients were instructed to take antiplatelet medication and statins (100mg/day of acetylsalicylic acid and 40mg/day of Simvastatin).Table 4 illustrates the patients' outcomes.

DISCUSSION
2][3] The typical pain described in chronic mesenteric ischemia was present in three cases in this series.Also, if there is an indication for an aortic or other abdominal procedure that could disrupt the collateral pathways, surgical reconstruction is indicated, as done in the patient in case four, who was operated prophylactically during an open AAA procedure. 1She presented with atypical postprandial pain, but she also gained 5kg after the operation and enlargement of the proximal segment of Riolan's arcade was evident, as seen in the control CTA 1 year after the revascularization.
Duplex ultrasound can be used as first screening imaging modality for diagnosis of CMI. 8 However, CTA is the primary imaging modality, with sensitivity and specificity of 95% to 100% for mesenteric arterial occlusions and it enables identification of collateral pathways. 1It is also indicated for evaluation of associated arterial pathologies, such as obstruction or dilatation, and is used for planning surgery. 1 A multidisciplinary team plays a key role in the preoperative scenario, to better assess the patient's clinical conditions and nutritional status and to confirm the diagnosis using functional tests in selected cases. 8At our centers, all patients were evaluated by experienced gastroenterologists, cardiologists, pneumologists, vascular surgeons, and interventional radiologists.
The endovascular-first recommendation is consistent with several practice guidelines and there are studies supporting use of routine mesenteric stenting instead of plain balloon angioplasty, specifically, use of covered stents. 9,10owever, there is a lack of consensus regarding the exact threshold for deciding to opt for open revascularization and the greatest challenge is to select patients who will benefit from this treatment. 8,11linical risk stratification is the first step to guide the decision on treatment approach.Definitions of "high-risk" and "low-risk" patients are largely variable between studies and reporting standards are inconsistent.Use of a previously validated tool, such as the Society for Vascular Surgery score, can be helpful to establish this classification. 12This is a simple algorithm based on patients' age, pulmonary and cardiac dysfunction, and renal insufficiency, in which patients are classified into low-risk or high-risk categories by the presence of at least one of the high-risk criteria defined. 12All of the patients in our study were classified as "low-risk" and so open revascularization could be attempted.
The second imperative principle for open revascularization is the anatomic pattern.There are some specific conditions in which the endovascular technique may be unfeasible, such as flush aortic occlusions, long segment occlusions (>2cm), severe calcification, tandem lesions, distal lesions, and small diameter vessels. 8,9An additional potential contraindication to the endovascular approach is the situation in which open revascularization is performed prophylactically during open procedures that could disrupt collateral pathways, such as open AAA repair with previously diagnosed mesenteric stenosis, as presented in case number four.
The endovascular technique is rapidly evolving and some authors have described endovascular strategies to overcome these barriers. 13Sharafuddin et al. 13 reported their experience with 27 patients with total mesenteric vessel occlusion with promising results regarding technical success rate (85%).Nevertheless, the 1 and 3-year primary patency rates were disappointing (58% and 33% respectively).Additionally, 2 patients died in this series.On the other hand, open repair is definitely durable with a 5-year primary patency of 88% in some series. 12These results reaffirm that the anatomical threshold has yet to be crossed and the role of endovascular treatment for these higher risk anatomic lesions is not firmly established. 14,15Also, the need for reinterventions must be discussed during patient counseling in order to assist the treatment choice. 12,16,17he most challenging situation is to select optimal treatment in high-risk patients with high-risk anatomic lesions.Some authors support initial stenting as a bridge therapy so that open surgery can be performed later, or repeated interventions to provide short-term symptom relief for patients with short life expectancy. 17,18ther groups believe that the open surgical approach performed retrograde (using the iliac artery as the inflow source) and avoiding aortic clamping can be performed safely as a good option for this group of patients. 12,16This technical solution was performed in patient #3 with good results.
There is also a discussion regarding the number of arteries that need to be treated.When performing angioplasty, there is a tendency to treat all three trunks, even though there is a preference for the SMA. 19uring open revascularization, the literature shows good results with revascularization solely of the SMA, with long term results similar to performing grafts for more than one trunk. 20,21inally, the choice of treatment approach may be not so elementary as a simple issue of endovascular or open first.The decision must involve patient clinical risk stratification by a multidisciplinary team, detailed anatomic profile, individual goals of care, surgeon experience, and patient decision.An algorithm for CMI management based on the authors' experience and an extensive literature review is proposed in Figure 4.
In this series, all patients demonstrated resolution of the ischemic symptoms and body weight recovery.All grafts are patent after a mean follow-up of 2 years.The series draws attention to the simultaneous occurrence of other arterial manifestations related to the degenerative process of atherosclerosis, such as: renal artery, carotid, and lower limb occlusions, and the presence of dilatation of aortic segments, which is in consonance with the existing literature. 22Nonetheless, the open revascularization procedures achieved good results, with low procedural mortality, just as the literature indicates for selected patients, reaffirming the utmost importance of open revascularization in CMI, even in the endovascular era. 23he limitations of the present study include its retrospective design with a small number of patients and a relatively short follow-up period.

CONCLUSION
Open repair using the C-loop configuration is a feasible technique for CMI with good results in selected cases.The algorithm constructed may help decision planning at other centers.
with a reinforced PTFE graft from the graft to the SMA Reinforced PTFE graft from the right iliac artery to the SMA Polyester aortobiiliac graft for correction of an AAA with a reinforced PTFE graft from the right graft limb to the median colic artery at Riolan's arcade AAA = abdominal aortic aneurysm, PTFE = Polytetrafluoroethylene, RCC = red cell concentrate, SMA = superior mesenteric artery.

Figure 1 .
Figure 1.Intraoperative and imaging findings for patient #2.(a) Preoperative computed tomography angiography showing the superior mesenteric artery (SMA) and the inferior mesenteric artery occluded; (b) Intraoperative view of a polyester aortobifemoral graft with a reinforced PTFE graft from the aortic graft to the SMA.

Figure 2 .
Figure 2. Intraoperative and imaging findings for patient #3.(a) Preoperative computed tomography angiography (CTA) with celiac trunk stenosis.The superior mesenteric artery (SMA) and the inferior mesenteric artery are occluded; (b) Postoperative CTA with a patent reinforced PTFE graft from the right iliac artery to the SMA.

Figure 3 .
Figure 3. Intraoperative and imaging findings for patient #4.(a) Preoperative computed tomography angiography (CTA) with all 3 trunks occluded.Riolan' s arcade is filled by the left internal iliac artery; (b) Polyester aortobiiliac graft for correction of an abdominal aortic aneurysm with a reinforced PTFE graft from the right graft limb to the median colic artery at Riolan' s arcade; (c) Postoperative CTA showing the patent graft (highlighted in orange) and the polyester aortobiiliac graft (highlighted in purple).

Table 3 .
Details of surgical procedures.