Introduction 

Surgical and X-ray endovascular revascularization has taken the leading positions in the treatment of the ischemic state of various organs and tissues. Revascularization of the heart, the brain, the kidneys, the abdominal organs, the extremities, etc. has saved the lives of and returned to normal work many millions of people in the world. Today, there is no doubt that these procedures improve the clinical state of the patients, as well as the blood circulation in the arterial vessels after revascularization. The issues concerning the effect of reperfusion on the state of microcirculation in these organs have been studied to a much lesser extent. An example is the internal carotid artery (ICA) revascularization procedure. It is known that this vessel is responsible for the vascularization of a significant part of the brain, and the impaired blood flow in it may lead to significant and sometimes irreversible dysfunctions of the central nervous system. For example, stenosis of the carotid artery, and, thereby, impaired vascularization of the brain structures are among the most important risk factors for the development of ischemic strokes and transient ischemic attacks. It should be noted that about 15 – 25 % of the diseases of the nervous system are caused by impaired cerebral circulation. In economically developed countries, cerebral stroke ranks third among the mortality causes. It is known that about two-thirds of all ischemic stroke cases are caused by the steno-occlusive lesions of the carotid arteries. For instance, with a stenotic lesion of the ICA by more than 75 %, the likelihood of developing an ischemic stroke during the first year after the diagnosis ranges between 2 and 5 %, and in the presence of clinical manifestations in the form of transient ischemic attacks, the likelihood increases to about 40 %. It should be especially noted that the degree of stenosis of the carotid artery is a fairly clear indicator of the likelihood of a cerebral stroke in the patients, and serves as an objective indication for medical procedures on the vessel ^[1-3].

Until the end of the eighties of the past century, drug therapy had been mainly used for the treatment of the patients with stenotic lesions of the carotid arteries, while surgical treatment, namely, carotid endarterectomy (CEAE) had been used much less frequently. However, with the introduction of endovascular revascularization of the vessels into the clinical practice, this method has been successfully and widely used for the treatment of stenotic lesions of the carotid arteries. Today, one can confidently say that the main methods of treatment for the patients with clinical manifestations of cerebral vascular insufficiency and carotid stenosis are carotid artery stenting and carotid endarterectomy. In recent years, a sufficient number of randomized studies comparing the two methods in the treatment of the brachiocephalic vessels have been published. These studies have not revealed any significant differences in the immediate and long-term results of treatment with the use of these methods of brain revascularization ^[4]. Therefore, in such cases, preference should be given to the less traumatic method of treatment, which is stenting of the carotid artery.

In using either method of revascularization of the brain, the degree of impaired blood circulation correction efficiency both at the level of macrocirculation, i.e., the great vessels, and at the level of microvasculature remains the main issue. While concerning large vessels, the results of the treatment may be quite adequately assessed by computed tomography, magnetic resonance imaging, and ultrasound imaging, studying the microvasculature of the brain structures seems to be more complicated ^[5]. It should be noted, however, that in recent years, the methods that allow a fairly complete study of the blood circulation at the level of microcirculation have appeared. An example is a method of optical coherence tomography (OCT) which may be successfully used for studying the microcirculation of the ocular fundus, which is a structure of the brain, and at the same time, is sensitive not only to the circulatory disorders in the ICA system but also to the disruption of the blood supply to the heart ^[6].

OCT-A is a relatively new technology that allows non-invasive visualization of the vasculature of the retina and the optic nerve head (ONH) by assessing quantitatively and qualitatively the blood flow in these areas. It should be particularly noted that the blood vessels of the fundus are extremely sensitive in general to the pathological processes in the organism, and in particular, in the pathology of the brain, the nervous system, and the heart ^[7-9]. In particular, this applies to the processes associated with the impaired vascularization of these structures. It is known that steno-occlusive changes in the ICAs are accompanied by the impaired blood supply to the eyes, which in turn may lead to a sudden or progressive decrease in visual acuity. It is, therefore, logical to assume that reverse changes, i.e., improvement of the blood circulation in the ICA system, may be accompanied by positive changes in the microcirculation of the fundus, and the eye in whole ^{[10, 11]}.

That said, the task was set to study the microcirculation of the retina and the optic nerve trunk before and after restoring the adequate blood flow in the ICA by stenting or CEAE through OCT-A in the patients with a sharp (> 75 %) stenotic lesion of this vessel.

Materials and Methods

The study involved 30 patients with hemodynamically significant stenosis (≥ 75 %) of the right or left ICA. The patients had been divided into two groups: Group 1 — patients after stenting of the ICA (17 patients), and Group 2 — patients after carotid endarterectomy performed from the carotid artery (13 patients). The clinical characteristics of the patients are shown in Table 1.

As one can see from Table 1, multifocal atherosclerosis was observed in the absolute majority of the patients. Some of them had a history of direct myocardial revascularization and/or stenting of the coronary arteries. It should also be noted that 22 (73.3 %) patients had stenotic lesions of the other carotid artery of varying severity, which, however, did not exceed 70 %.

The criterion for involving the patients in the study was the presence of stenosis of the ICA (≥ 75 %). In most cases, the right ICA had been affected. The patients with severe ocular pathology associated with a reduced permeability of the optical media (cataract) or the presence of vitreoretinal diseases, as well as the patients with acute myocardial infarction and those with serious neurological diseases, including cerebral stroke, were not involved in the study.

Stenting of the ICA was performed following the standard technique with the obligatory use of an anti embolic protective device and balloon post-dilation of the stented area.

CEAE was performed under general anesthesia. After the isolation of the common carotid artery and bolus administration of heparin, the common, external, and the ICAs were separately clamped, and bypasses were placed above the vascular compression to maintain perfusion of the intracranial arteries. After that, the atherosclerotic plaque was removed. The duration of ICA clamping during the surgery averaged 28.4 ± 5.9 minutes. The patients were monitored within 24 hours after CEAE.

OCT-A was performed on a CANON tomograph using an A-scan with a capacity of 70,000 scans per second. The study was performed by the same researcher in completely identical conditions. The ONH area was 4.5 x 4.5 mm², and the macular area was 3.0 x 3.0 mm². The comparative analysis was performed for the surface capillary layers of the ONH and the macular area, as well as the deep capillary layer of the macula and the choriocapillaris layer of the ONH. The flow density segmentation was determined automatically for each area and subjected to further analysis.

Before OCT-A, the patients had remained at complete rest for five minutes, after which their blood pressure was measured on the left arm in a sitting position, provided that the patient's arm was exactly at the height of the heart. The patients underwent OCT three times in the following sequence: in Group 1, not earlier than one week before stenting and two-three days after the procedure; in Group 2, also not earlier than one week before carotid endarterectomy and five-seven days after it. Three months after the procedure, all patients in both groups underwent the third follow-up OCT-A on an outpatient basis.

Results

The OCT-A performed before revascularization procedures did not reveal any significant differences in terms of the blood flow density on the side of the stenosed and non-stenosed carotid arteries (p < 0.05). The groups were also comparable from the standpoint of baseline indicators (Table 2).

In the early postsurgery period, the blood flow density increased in the macular area both at the level of the surface and the deep layer (p < 0.05). It should be noted that the increase in the blood flow density was more pronounced in the area of the capillary plexus and the capillary choroid of the ONH (p < 0.01). The studied parameters obtained after stenting and carotid endarterectomy were not veraciously different (Table 3).

It should be particularly noted that an increase in the flow was also noted on the contralateral side (Table 4).

Figure 1 shows the data of OCT-A of the retina in patient O. 58 years old before and at various times after stenting of the right ICA.

The clinical example of changes in the retinal flow density in 57 years old patient after ICA stenting.

Figure 1: OCT angiogram of the patient before and after stenting of the right carotid artery. An improvement in the microcirculation three days and three months after the surgery is visible on the slices

At the follow-up examination three months after the revascularization procedures, OCT-A showed a moderate decrease in some flow density parameters, compared to the results obtained immediately after the procedure; however, they remained higher than the initial values, both on the affected (Table 5) and the contralateral side (Table 6).