Chronic mesenteric ischemia (CMI), which is characterized by such manifestations as non-specific abdominal pain after a meal and weight loss that affects patients’ nutrition, can develop into acute mesenteric ischemia, which is a dangerous and often lethal disease. Still, CMI remains an understudied, often non-diagnosed and non-treated disease. This primarily occurs because of the lack of respective knowledge in the medical society. It is suggested that an increase in life expectancy, rate of cardiovascular diseases among the senior population, and metabolic disorders will contribute to an increase in the occurrence rate of CMI. Modern methods of radio diagnostics and expansion of indications to these studies provided earlier and precise diagnostic of the disease and improved the disease outcome.

The review was aimed to evaluate the issue of CMI and modern possibilities of radio diagnostics, bolus contrast-enhanced multislice spiral computed tomography (CE-MSCT), or multislice spiral computed angiography (MSCT-A) to propose the interdisciplinary algorithm of monitoring for this group of patients as well as to compare the data on the most studied anomalies of abdominal vessels with their clinical picture, anatomy, and pathogenesis, to evaluate the main patterns that would help radiologists, physicians, gastroenterologists, vascular surgeons, general practitioners, and medical specialists that work with this group of patients.

A systematic review of the published studies was made according to standard recommendations. The authors searched publications made during the past decade in Russian and English language electronic databases PubMed, Google Scholar, Google books, Ciberleninka. The search was made for keywords that included “сhronic mesenteric ischemia, multislice spiral computed tomography angiography, atherosclerosis, fibromuscular dysplasia, vasculitis, and median arcuate ligament syndrome” in English language databases and “синдром хронической абдоминальной ишемии, мультиспиральная компьютерно-томографическая ангиография, атеросклероз, фиброзно-мышечная дисплазия, васкулиты, синдром внешней компрессии чревного ствола” in Russian language databases. The search for articles was performed in four directions that included atherosclerosis of the abdominal aorta and its unpaired visceral branches, fibromuscular dysplasia, vasculitis, and median arcuate ligament syndrome. All publications were checked for methodological validity before the inclusion in the article.

The peculiarities of CMI diagnostics are associated with non-specific symptoms such as abdominal pain, weight loss, altered defecation patterns, nausea, etc. [1].

It should be highlighted that apart from visualization of parenchymatous organs, a widely used ultrasonic investigation allows specialists to evaluate the blood flow in vessels. However, its application is limited in cases that are similar to ischemic vascular abdominal pathology because it cannot evaluate collateral blood flow, condition of parenchymatous organs in bolus-enhanced condition, and the status of intestinal walls [1][2].

CE-MSCT or MSCT-A are acknowledged methods of visualization of the first line due to its rate, availability, and capacity to diagnose alternative reasons for abdominal pain [3].

The technique of the study will vary depending on the chosen protocol.

The patient received orally 500-800 ml of contrast agent (water) for stomach and small intestinal contrast. A total of 100-120 ml of Iodine-containing contrasting agent was injected in the ulnar vein with an injector (18-20G) at the rate of 4-5 ml/s for adequate evaluation of the arterial and venous systems. The arterial phase imaging (25-30 seconds after the injection of the contrast agent) was obtained from the level above the celiac trunk to the level of common iliac arteries. The portal vein phase imaging (60-70 seconds after the introduction of the contrast agent) was obtained from the level above the diaphragm and below the pubic symphysis [4][5].

The collected and analyzed data was processed with a special working station and included 2D multiplanar images, maximum intensity projection (MIP), and volumetric rendering (VR) for 3D images of blood vessels [6][7].

MSCT-A images were checked for arterial stenosis or occlusion. For example, vascular occlusion is defined as a complete lack of lumen contrast, hemodynamically significant vascular stenosis was defined as a reduction of the lumen diameter to >50%, and hemodynamically insignificant stenosis is a reduction of lumen diameter to <50% [6].

There is also another point of view. Patients with abdominal ischemia symptoms and damage of one vessel of the celiac trunk or the upper mesenteric artery stenosis to ≥70% can be considered significant. In patients with manifested symptoms of vast lesion of the upper mesenteric artery and its branches, stenosis to ≥50% can be considered significant [8].

The most common secondary signs of ischemia on CT images included thickening of the intestinal wall, focal lack of intestinal wall contrasting, dilatation of the intestine, ascites, intestinal pneumatosis, free gas in the peritoneal cavity, and infarction of the parenchymal organs [8]. General contraindications to CE-MSCT were pregnancy, previous severe reactions to the contrast agent, claustrophobia, and lack of contact with a patient [7][9][10].

There were no publications on a direct comparison of CE-MSCT and MRI of mesenchymal vessels. For renal arteries, it was shown that MSCT-A was more informative than CE-MRI angiography [9]. The sensitivity of MSCT-A for the diagnostic of mesenchymal ischemia was 100%, the specificity was 95–100% [1].

Chronic mesenteric ischemia includes stenosis-induced or occlusion-induced ischemia, vasculitis (Takayasu’s arteritis (TA), segmental arterial mediolysis (SMA)), and celiac axis compression syndrome [11].

The cause of pain syndrome is mesenteric ischemia induced by a direct ischemic effect with further pain mediator release as well as “steal syndrome” with respective pathogenetic mechanisms of pain syndrome development [12][13].

The most common causes of CMI include atherosclerotic occlusion or severe stenosis of mesenteric arteries. Stenosis to >50% is observed in 18% of patients older than 65 years old. However, only some of them have manifested symptoms [14].

Nearly in 50% of patients with atherosclerotic damage of peripheral or coronary vessels, a lesion of non-paired branches of the abdominal aorta is observed [15]. According to Krishnamurthy et al., angiography reveals clinically significant stenosis of two and more mesenteric arteries in 20.4% of patients with ischemic heart disease [16]. The occurrence rate of atherosclerosis of the abdominal aorta in patients with atherosclerosis of lower extremities was evaluated in some publications. According to some authors, it reached 60-100% and correlated with the expression of stenosis in both vascular pools [17][18].

The symptoms occur after a meal, which is associated with an enhancement in the blood flow, and are manifested as a classic clinical triad (postprandial abdominal pain, weight loss, and food refusal) that is observed in nearly half of patients with chronic mesenteric ischemia [19][20]. The main three non-paired arteries that arise from the abdominal aorta are the celiac artery, superior mesenteric artery (SMA), and inferior mesenteric artery (IMA). Since a collateral blood flow is present at several levels, patients might not experience symptoms even in the case of stenosis of several arteries simultaneously. When SMA is occluded, pancreaticoduodenal arteries feed the intestine via the hepatic and gastroduodenal arteries. When the celiac artery and SMA are occluded, the small intestine is fed from the IMA pool via the left colic branch. The symptoms usually arise from stenosis and/or occlusion of two and more vessels, although there are exceptions to this rule [21][22].

This pathology is usually diagnosed with CT angiography without issues. Atherosclerotic deposits are primarily localized in the entrance of the celiac artery and SMA [22].

A clinical example from the author’s archive data is presented in Fig. 1.

Non-atherosclerotic causes of structural changes in the vascular wall include fibromuscular dysplasia (FMD). It is a rare but well-known cause of chronic mesenteric ischemia [23].

FMD is a heterogeneous group of vascular pathology that is characterized by idiopathic, non-inflammatory, and non-atherosclerotic angiopathy of small and medium arteries [23][24]. The prevalence of this pathology is unknown. Most commonly, it is diagnosed in young women aged 30 to 50 years old [25][26].

FMD can develop without the manifestation of symptoms. The developed symptoms can be associated with renal arteries pathology (hypertension or failure caused by the renal artery stenosis) caused by the lesion of the carotid and vertebral arteries (impulse noise, transitory ischemic attack, stroke), and coronary artery lesion (angina, infarction) [26][27][28]. The expressed clinical manifestations of mesenteric ischemia develop early rarely because of collateral blood supply [28].

Structural changes in the vascular walls are associated with fibrous or fibromuscular thickening. Any layer of the vascular wall can be affected (intima, media, or adventitia) without the signs of inflammation [25][26][29][30].

In 90-95% of cases, the media is affected. As a result, in most cases, stenosis develops with areas of expansion (small aneurysms). Less frequently, uniform stenosis of the vascular wall develops. FMD “weakens” the vascular wall, which contributes to the formation of the arterial wall dissection [26][31].

It can affect any medium-size artery and is primarily characterized by a bilateral localization (for example, in the case of the renal artery lesion) with the involvement of several arteries. The complications can include spontaneous dissection, distal embolization of the clot formed in the cases of an aneurysm, and hemorrhage. Digital subtraction angiography remains the gold standard of FMD diagnostic because it allows specialists to visualize minor or peripheral lesions. A specific feature of the most common medial type is an alternation of stenosis and dilatations that is called a string of beads sign. Less frequently, intimal and adventitial types are characterized by focal concentric stenosis of long segments or diverticular bulging. The advantages of MSCT and MRI are in the possibility to evaluate the ischemic lesion of the abdominal organs [28][31][32].

Typical angiographic signs include vascular loops, fusiform vascular ectasia, a string of beads, and stenoses. Fig. 2 shows an example of FMD from the authors’ archive.

Differential diagnosis during the visualization includes atherosclerosis, usually in the beginning or in the proximal part of the artery, vasculitis, elevated ESR +/- fever, traumatic iatrogenic damage of the vessels (possible segmental arterial mediolysis) [26][28][31].

The most common condition among vasculitis and connective tissue diseases that causes chronic mesenteric arteritis is Takayasu arteritis [33]. Takayasu arteritis (АТ) is known as idiopathic arteriopathy. It is granulomatous vasculitis of large vessels that primarily affects the aorta and its main branches, and sometimes, pulmonary and coronary arteries [34][35]. The causes of the disease are unknown, however, it is considered that this pathology is similar to giant cell arteritis. This pathology prevails in women (<50 years old). The typical age of symptoms manifestation was 15-30 years old. Some researchers highlight the facts of geographical coincidence of the cases of tuberculosis and Takayasu arteritis, which suggests an association between these diseases. Probably tuberculosis causes an immune-mediated reaction of large vessels. Still, this hypothesis remains controversial [34].

Takayasu arteritis classification (Numano) [36]:

The lesion of coronary and pulmonary arteries are marked as C(+) or P(+), respectively.

The clinical picture includes various ischemic symptoms caused by stenosis or clot formation. First symptoms are usually manifested as fatigue, fever, night sweats, weight loss, and arthralgia. Frequently, anemia with elevated levels of inflammatory markers is observed. This phase resolves with the beginning of the chronic phase that is characterized by inflammatory and obliterating alterations in the aorta and its branches. Peripheral pulse often decreases or is absent. For this reason, this disease is also called a “pulseless disease”.

CT-picture presents a uniform and expended thickening of the intestinal wall. In the active phase, enhanced contrast of the intestinal wall, stenosis, occlusion of the main aortic branches, aneurysmal dilatation of the aorta or its branches, and formation of pseudoaneurysm can be observed [37][38][39].

Fig. 3 presents an example of a CT image of Takayasu arteritis.

A group of rare vasculitides, that lead to chronic mesenteric ischemia, also includes segmental arterial mediolysis (SAM), which is considered to be a rare arteriopathy [9]. The main histological process of SAM is the lysis of smooth muscles of the arterial wall, which leads to the intramural hemorrhage, sacculated or dissecting aneurysm, thrombosis, or hemorrhage [40][41].

SAM primarily affects medium branches of the superior mesenteric artery. The etiology of the disease is unknown but there is an association observed with episodes of internal vessel narrowing (for example, shock, hypoxia, recent vast surgery, vasopressor infusion) [40][42][43]. There is some histologic similarity with FMD, which is considered to be a differential diagnosis, but clinical signs and distribution of lesions are usually typical.

Lately, the occurrence rate of the disease increased due to a wider implementation of CT angiography and awareness-raising in the radiological society. The morbidity rate can reach up to 1 case per 100,000 patients per year [40][43].

Abdominal pain, distention, shock in severe cases, and hematocrit fall are typical symptoms. In middle-aged patients with non-traumatic spontaneous mesenteric hemorrhage, segmental arterial mediolysis is the most probable primal cause. In acute cases, the lethality rate is up to 50% [43].

CT picture is characterized by fusiform aneurysms, stenosis, dissections, and occlusions of arteries. A sequence of aneurysms and stenosis (string-of-beads sign) is observed. Their distribution tends to avoid bifurcations [42].

An example is presented in Fig. 4.

The causes of external impact on abdominal vessels that lead to the development of mesenteric ischemia include median arcuate ligament syndrome (Dunbar syndrome or Harjola-Marable syndrome), which is characterized by external compression of the celiac trunk by the diaphragmatic crurae [44]. There is no consensus on what should be considered a pathology and what is variant anatomy because this anomaly is met in symptomless patients [45][46].

In 10–24% of patients, the ligament can go in front of the artery. In some of them, the ligament compresses the celiac artery, which impairs the blood flow and provokes symptoms [47]. The expressed compression develops nearly in 1% of patients and persists during inhaling [48]. Its occurrence rate is higher in women (mean age is 30-50 years old) and slim patients [46]. Clinical symptoms include position-dependent chronic pain in the abdomen, especially after a meal, which intensifies in the supine position at the expiratory height, nausea/vomit, and weight loss [46].

It is suggested that the etiology of abdominal pain is ischemic. It is caused by blood flow failure caused by compression. Alternatively, it was suggested that there was a neuropathic component associated with an impact on the celiac plexus [46].

CT picture of the celiac trunk compression includes a focal narrowing of the upper proximal celiac trunk section, which has a hooked or J-like appearance, signs of collaterals, and lack of associated atherosclerosis. CT-angiography is used additionally to evaluate post-stenotic dilatation, branches of the celiac trunk (gastroduodenal and common hepatic artery), and thickening of the median arcuate ligament. The thickness of the median arcuate ligament of more than 4 mm is considered to be abnormal [46].

Often, the breathing phase significantly affects the degree of the celiac trunk narrowing. Primarily, stenosis is more expressed at the end of exhaling and less expressed at the end of inhaling. Thus, it is recommended to visualize during the final inhale to reduce the possibility of detection of clinically insignificant narrowing (false positive) [49][50]. Examples of celiac trunk compression stenosis and combined vascular pathology from the authors’ archive are presented in Figs. 5 and 6.

CE-MSCT or MSCT-A is a preferable method for the diagnostic of structural changes in patients with pain syndrome and suspected chronic mesenteric ischemia. It allows specialists to evaluate the condition of vessels as well as post-ischemic alterations in the visceral organs.

In patients with non-specific gastrointestinal complaints (chronic pain syndrome after a meal, weight loss, etc.) and lack of evident cause and effect relation with visceral pathology, chronic mesenteric ischemia should also be excluded.

Clinical specialists should discuss diagnostic tactics with radiologists when selecting the optimal method of diagnostics.

Frequently, an occlusive form of mesenteric ischemia in patients older than 65 years old is caused by atherosclerotic changes in unpaired aortic branches. Primarily, the symptoms appear when two or more branches are affected.

When patients have complaints typical for ischemic pain syndrome and verified atherosclerotic damage of coronary and lower extremity arteries, there is a high risk of occlusive lesion of the abdominal aorta branches.

Rare non-atherosclerotic causes of vascular lesion that lead to mesenteric ischemia include vasculitides (Takayasu’s disease, segmental arterial mediolysis) and FMD.

When patients have complaints typical for mesenteric ischemic syndrome in combination with a typical lesion of renal arteries and unpaired abdominal aorta branches, FMD should be excluded.

When a patient has signs of chronic mesenteric ischemia after vast surgical interventions in the anamnesis that were associated with shock, hypoxia, and injection of vasopressors, segmental arterial mediolysis should be excluded.

Young patients with suspected mesenteric ischemia and position-dependent abdominal pain with a typical narrowing of the celiac trunk proximal segment and hypertrophy of the diaphragm crurae might have median arcuate ligament syndrome.