Introduction

Acute mesenteric ischemia (AMI) is caused by acute decrease or cessation of oxygen delivery to intestinal tissues due to acute occlusion of great mesenteric arteries or veins. Arterial form of AMI following acute occlusion of superior (SMA) or inferior mesenteric (IMA) artery is the most important regarding disability and high mortality rates (≥60–70%) [1–3]. Despite modern methods of diagnosis and treatment, mortality rates did not decrease over the past 15 years [4, 5].

The main causes of high mortality are still difficulties in clinical and laboratory diagnosis of disease, comorbidities in advanced age patients, extensive intestinal necrosis with abdominal sepsis, reperfusion injuries, bacterial systemic translocation, progression of intestinal necrosis in postoperative period and others [5-7]. In most cases, surgeons encounter thromboembolism or thrombosis of SMA followed by subtotal ischemia and necrosis of small bowel and right half of the colon. Successful revascularization of intestine and resection of necrotic tissues per se do not yet guarantee success in treatment, since postoperative period may be complicated by abdominal sepsis, reperfusion and translocation syndrome. These events significantly worsen treatment outcomes [8—11].

The purpose of the study was to describe 15-year experience in surgical treatment of arterial form of AMI, as well as to demonstrate modern epidemiological data on this disease in a single multi-filed hospital during the same time.

Material and methods

There were 407 patients with AMI between 2007 and 2022. Venous portomesenteric thrombosis as a cause of intestinal ischemia and abdominal pain was found in 22 (5%) patients. In other 385 (95%) patients, acute occlusion of SMA or IMA was the cause of ischemia of small and large bowel. In the future, we will analyze only these 385 patients with arterial form of AMI.

The causes of AMI (based on clinical data, cardiac arrhythmias, intraoperative data and morphological data) were distributed as follows: SMA thromboembolism — 196 (51%) patients, SMA thrombosis — 164 (43%) patients. The cause of colon necrosis in other 25 (6%) patients was acute occlusion of IMA. Female patients prevailed (258/67%), there were 127 (33%) males. Age of patients ranged from 41 to 97 years (mean 74±9).

Cardiovascular diseases included hypertension with complications (89%), coronary artery disease (61%), and atrial fibrillation (48%). Previous myocardial infarction or ischemic stroke was observed in 38% of patients. Twelve (3%) patients underwent surgery in acute period of myocardial infarction or ischemic stroke, i.e. these patients developed AMI in the hospital.

The main diagnostic method for AMI was CT angiography.

All 385 patients with arterial AMI underwent surgery. Intestinal revascularization was performed in 101 patients (open embolism or thrombectomy from SMA — 10 patients, endovascular intervention — 41 patients, small intestine revascularization with resection of necrotic tissues — 50 patients). Isolated resection of necrotic intestine was performed in 176 patients. Explorative laparotomy was performed in 108 patients with total intestinal necrosis.

Extracorporeal detoxification for reperfusion syndrome included high-volume veno-venous hemofiltration and hemodiafiltration in intermittent mode. Twenty-seven (7%) patients underwent 1-5 procedures.

Data in the article are presented in absolute and relative values.

Results and discussion

AMI is accompanied by complete occlusion of the great mesenteric vessels and includes SMA thromboembolism (40–50%), SMA thrombosis (15–30%) and venous portomesenteric thrombosis (5–15%). Arterial form of AMI following SMA thromboembolism or thrombosis is of the greatest importance due to high mortality rates [2, 12].

Among 407 patients for 15 years, there were 385 (95%) patients with arterial AMI. Other 22 (5%) patients had portomesenteric venous thrombosis.

SMA embolism caused intestinal ischemia in 51% of patients, SMA thrombosis — in 43% patients. However, if we consider 25 (6%) patients with acute occlusion (thrombosis) of IMA, proportions of embolism and thrombosis of visceral arteries as the causes of AMI become approximately the same (51% vs. 49%).

Our own epidemiological data on the incidence of AMI in the same hospital in different cohorts of patients, as well as comparison of our findings with the world data are presented in Table 1.

Table 1. Prevalence of acute mesenteric ischemia

According to Table 1, our own epidemiological data basically coincide with foreign reports.

According to the literature, incidence of AMI is higher in older patients [15-17]. For example, abdominal pain may be caused by AMI in 10% of patients over 70 years old. According to other data, incidence of ischemia or intestinal necrosis in suspected acute appendicitis is 2.1%. AMI is detected in 17.7% of cases after emergency laparotomy and in 31% of patients with non-traumatic diseases undergoing damage-control laparotomy.

As you known, one of the main factors regarding AMI-related mortality is time from admission to diagnosis and surgical treatment. Immediate diagnosis and emergency surgery are accompanied by mortality up to 10%. In case of delayed surgical treatment for more than 24 hours, this value is up to 80-100% [18]. In this regard, the main and early diagnostic method for suspected AMI should be contrast-enhanced CT.

Intestinal revascularization is common for acute occlusion of the orifice and/or proximal segments of SMA. In our group, 101 patients underwent intestinal revascularization (isolated open embolectomy or thrombectomy (n=10), endovascular interventions (n=41), combination with resection of necrotic segments (n=50)). The need to restore blood supply is due to the main factor because early revascularization ensures the viability of ischemic or residual intestine. For example, Tran L.M. et al. [3] showed that delayed vascular examination and bowel revascularization are independent risk factors of 30-day mortality. Moreover, delayed revascularization of SMA extends intestinal resection and contributes to short bowel syndrome in long-term period. Other authors also emphasize the role of early intestinal revascularization as a key to success in effective treatment of AMI [19].

Indications, prospects, possibilities, comparability of results and certain advantages of endovascular techniques over open SMA revascularization are actively discussed in the world literature [2, 20, 21]. The need for bowel resection after endovascular intervention occurs in 36-45% of cases, and mortality rates vary from 12 to 46% [7, 21, 22].

The first successful endovascular SMA revascularization for AMI was performed in our clinic in 2008. However, the main experience of these operations for acute occlusion of SMA has been accumulated since 2013. To date, 41 endovascular operations have been performed in patients with AMI (15% of all interventions).

Considering own experience and world literature data, we established the indications for endovascular treatment of AMI:

— clear consciousness;

— no peritoneal symptoms;

— no data on perforation of a hollow organ;

— no CT signs of intestinal necrosis (free gas in intestinal wall or mesenteric vessels);

— no inotropic or vasopressor support at admission and before surgery, i.e. stable hemodynamics.

Technical success with complete angiographic restoration of blood flow in SMA and large tributaries was achieved in 85% of cases (35 out of 41 patients). At the same time, complete restoration of arterial blood flow after balloon angioplasty and thrombo- or embolectomy was achieved in 15 patients. In other 20 cases, angioplasty and aspiration were supplemented with SMA stenting for significant residual stenosis (preservation of remnants of thrombotic masses or emboli).

In our opinion, elective laparoscopy 6-12 hours after successful revascularization is essential component after endovascular correction of mesenteric blood flow. This procedure is necessary to confirm viability of intestine for extracorporeal detoxification in reperfusion syndrome.

We encountered unfavorable complications such as reperfusion and translocation syndromes in early postoperative period after successful endovascular revascularization in these patients [8, 11]. The following mechanism of these syndromes is described in detail. Many active substances enter systemic circulation through the endothelial and epithelial barrier of intestine affected and destroyed by ischemia (bacterial intestinal microflora, pro-inflammatory cytokines, neutrophils, inflammatory mediators, reactive oxygen species, immune cells, various other oxidizing factors). The main target organ for these substances is lungs. In addition, reperfusion syndrome can lead to death from septic shock and multiple organ failure even before intestinal necrosis [8–11, 23].

In most of our patients, reperfusion syndrome was manifested by violation of central hemodynamics with decrease in cardiac output, total peripheral resistance and global diastolic end volume measured by transpulmonary thermodilution. In these patients, metabolic acidosis was accompanied decrease of blood pH, base deficiency and lactatemia. Importantly, transpulmonary thermodilution revealed increase in extravascular fluid in lungs. Finally, severe pulmonary edema and acute respiratory distress syndrome led to disruptions in gas exchange with development of hypoxemia, intracellular and tissue hypoxia, and irreversible metabolic changes. All these mechanisms caused 15% mortality (n=6) despite viable bowel.

Methods of extracorporeal hemocorrection (veno-venous hemofiltration and hemodiafiltration) used for extrarenal indications after successful intestinal revascularization were aimed at correcting systemic inflammatory response, restoring immune homeostasis, organ protection, correcting metabolism and water-electrolyte imbalance. There were 1-5 procedures. Extracorporeal detoxification procedures were performed in 27 patients, and the main indication was effective intestinal revascularization.

Intravenous anticoagulation with unfractionated heparin was administered to all patients. Anticoagulation per se was an independent factor improving prognosis and survival in patients with AMI. In addition, the advantages of unfractionated heparin are available titration for target hypocoagulation and possible block of effect for emergency and redo surgery [2]. Among 277 postoperative patients (108 exploratory laparotomies were not taken into account), the need for emergency redo laparotomy (redo laparotomy "on demand" for intra-abdominal bleeding under anticoagulation) occurred only in 3 (1%) patients.

In total, bowel resection was performed in 254 (66%) patients (extensive resection (> 2 m) — 29% of patients, non-extensive resection — 71% of patients). Elective redo laparotomy within 41±12 hours in 85 patients revealed intestinal necrosis (after isolated revascularization) or progression of necrosis after resection in 50 (59%) out of 85 patients. This required bowel resection with interintestinal anastomosis or repeated obstructive resection with postponing the decision on anastomosis until the second redo laparotomy.

Combined embolism of other great arteries is common in patients with acute thromboembolic occlusion of SMA that undoubtedly worsens prognosis and outcomes of disease and sometimes requires simultaneous open or hybrid revascularization [1, 24]. Incidence of combined embolism can reach 70%. Acosta S. et al. [24] analyzed autopsy material in 213 patients and revealed simultaneous arterial thromboembolism of other vascular systems in 68% of deceased patients. Shchegolev A.A. et al. [1] demonstrated successful hybrid intervention in a 95-year-old patient with simultaneous embolism of femoral and superior mesenteric arteries. The authors performed open embolectomy from lower limb arteries and endovascular embolectomy from SMA. In our group, combined symptomatic embolism occurred in 19 (5%) patients (thromboembolism of brachiocephalic arteries with ischemic stroke in 8 patients, thromboembolism of the great arteries of the upper or lower extremities with simultaneous revascularization of limbs or thromboembolism of other tributaries of abdominal aorta (celiac axis, splenic and renal arteries) in 11 patients).

The main postoperative complications were progression of intestinal necrosis (59%), inflammatory pulmonary complications (8%) and gastrointestinal bleeding (3%). Other complications (myocardial infarction, ischemic stroke, pulmonary embolism, intra-abdominal bleeding, postoperative wound suppuration) comprised <3%.

The algorithm used in patients with suspected AMI is shown in the Figure.

Treatment and diagnostic algorithm for acute mesenteric ischemia.

Mortality in acute occlusion of IMA

Mortality among patients with acute IMA occlusion was 88% (22 out of 25 patients with colonic necrosis died). The main causes of high mortality rate were senile age of patients, comorbidities, multifocal critical atherosclerotic lesion of other arterial pools (cerebral and cardiac). Most of these patients admitted with colon perforation, diffuse fecal peritonitis and severe abdominal sepsis.

Mortality in acute occlusion of SMA

Overall 15-year surgical mortality (277 operated patients and 108 patients with total intestinal necrosis) in acute SMA occlusion was 71% (256 out of 360 patients). Postoperative mortality excluding exploratory laparotomies over the same period was 59% (148 patients).

Data on in-hospital mortality in AMI are summarized in Table 2.

Table 2. Results of surgical treatment of acute mesenteric ischemia following acute SMA occlusion

Routine CT angiography of mesenteric vessels in case of suspected AMI, active and effective early intestinal revascularization including endovascular techniques, introduction of extracorporeal hemocorrection for the treatment and prevention of reperfusion and translocation syndrome have made it possible to achieve mortality rate of 49% over the past 10 years (2013-2022). Indeed, AMI-related mortality rate within the first 5 years (2007-2012) was 64% (p=0.16) (Table 2).

Conclusion

AMI remains a disease with high mortality and extremely poor prognosis. Early diagnosis of AMI using modern diagnostic methods (CT angiography of mesenteric vessels), effective SMA revascularization (open, hybrid or endovascular), prevention and treatment of reperfusion syndrome can improve postoperative outcomes.

The authors declare no conflicts of interest.