Anatomical and procedural predictors affecting the outcomes of flow diversion and endosaccular coiling in small saccular aneurysms of the internal carotid artery: a comparative cross-sectional study

Introduction

Saccular intracranial aneurysms (sIAs) affect 2% to 5% of the adult population and are the most common cause of non-traumatic subarachnoid hemorrhage (SAH). Aneurysmal SAH accounts for approximately 30% of hemorrhagic strokes and represent the leading cause stroke-associated death in young and middle-aged adults. The incidence of aneurysmal SAH is estimated at 10 to 20 cases per 100,000 population annually (1,2). This is a life-threatening condition with mortality rates up to 40% and morbidity up to 50% underscoring the need for preventive surgical treatment of unruptured sIAs (3).

The majority of sIAs are small (less than 10 mm in size) and located in anterior circulation. Although these aneurysms have relatively low annual risk of rupture, their high prevalence makes them responsible for most cases of aneurysmal SAH (4).

An endovascular approach is often preferred for preventive treatment of small unruptured sIAs. The standard endovascular technique is endosaccular coiling (EC) which may be supplemented with the use of intracranial balloons [balloon-assisted coiling (BAC)] and stents [stent-assisted coiling (SAC)]. The main concern with the EC is relatively low aneurysm cure rates: 20% to 50% of lesions do not sustain total occlusion, 10% to 30% of aneurysms ultimately require retreatment (5). Assisting techniques improve the effectiveness and enhance the technical capabilities of EC, but carry additional manipulation-related risks, which may be a critical issue in previously asymptomatic patients with incidental sIAs (6,7).

An alternative technique for treating sIAs is flow diversion (FD). Flow diverters demonstrated better outcomes in managing large, giant, fusiform and other aneurysms that are difficult to coil (8). Over the past decade, the use of FD has also increased for small sIAs amenable to coiling (9,10). However, the advantages of FD in this type of lesion are not yet well-established and require further investigation. Among the disadvantages of FD are delayed occlusion of the aneurysm, the requirement for double antiplatelet treatment (DAPT) and lower cost-effectiveness compared to EC in smaller lesions (11).

Aneurysms located in the intradural segment of the internal carotid artery (ICA) represent a special case. They account for approximately 30% of all sIAs and most can be effectively treated using both EC and FD. Investigating the surgical and anatomical features that influence the outcomes of EC and FD could provide an insight into which method is more suitable depending on specific characteristics of the target aneurysm. We did not find any studies that examine these factors in a comparative manner. We present this article in accordance with the STROBE reporting checklist (available at https://jni.amegroups.com/article/view/10.21037/jni-25-5/rc).

Aim

The objective of this study was to assess the procedural and anatomical predictors associated with target aneurysm non-occlusion when treated with EC and FD in small sIAs located at the intradural segment of the ICA.

Methods

The study represents a retrospective cross-sectional evaluation of imaging data and medical records obtained in single institution (E.N. Meshalkin National Medical Research Center, Novosibirsk, Russia) between August 2016 and July 2022. All patients treated consecutively during this period were screened for the following inclusion criteria:

• Saccular morphology of target aneurysm;
• Target aneurysm size 4 to 10 mm (max dimension);
• Aneurysm location at intradural segment of ICA (clinoid segment to ICA bifurcation);
• Unruptured or ruptured >30 days ago;
• Previously untreated.

All cases that met these criteria and had follow-up imaging available were enrolled into the study. The study flow chart is presented in Figure 1.

Figure 1 Study design flowchart. AR, aspect ratio; DSA, digital subtraction angiography; EC, endosaccular coiling; FD, flow diversion; IA, intracranial aneurysm; ICA, internal carotid artery; NMRC, National Medical Research Center; NTDR, neck-to-dome ratio; SR, size ratio.

All patients had a previously confirmed diagnosis of sIA, verified using CT-angiography, magnetic resonance (MR)-angiography or digital subtraction angiography (DSA).

The selection of the treatment modality was determined through a collaborative discussion of the initial imaging findings; however, the final decision was up to the operating interventionist in each case. This choice was based on interventionist’s experience and personal preferences, with respect to target aneurysm location and anatomical features.

All procedures were conducted under general anesthesia utilizing the biplane angiosuites, specifically the Philips Allura 20/20 (Philips Medical Systems Nederland BV, Best, the Netherlands) and GE Innova (GE Healthcare, Chicago, USA). Vascular access was established via femoral artery using short and long sheaths of 6 to 8 French and 13 to 80 cm in length. Intracranial approach was achieved using general purpose guiding catheters of 6 to 8 French and 90 to 125 cm in length. Flow diverters from variable manufacturers (refer to Table 1) were delivered via special-purpose microcatheters of 2.7 French. Detachable coils from multiple brands were introduced through general-purpose neurovascular microcatheters of 1.7 French. BAC and SAC were employed at the discretion of the operators. Non-flow diverter stents were delivered using reinforced microcatheters of 2.1 French (for high-profile stents) or 1.7 French (for low-profile stents). After the procedure the patients were monitored in neuro-intensive care unit (ICU) for 12 to 24 hours and, if uneventful, discharged home 2 to 3 days post-operatively.

Prior to the procedure all patients received mandatory DAPT: clopidogrel 75 mg daily or ticagrelor 90–180 mg daily, and aspirin 80 to 120 mg daily. Platelet function testing was performed for all patients using light transmission aggregometry (LTA) with adenosine, aiming for the platelet activation level of less than 30% from baseline. For patients who did not receive stents, DAPT was discontinued immediately after procedure. The stented patients continued DAPT for 4 to 6 months postoperatively.

All patients were scheduled for follow-up DSA between 6 and 12 months postoperatively. Those who did not undergo the follow-up DSA were excluded from the outcome assessment.

The angiographic outcomes were dichotomized into total occlusion (or “complete” occlusion) and non-occlusion (or “incomplete” occlusion). Total occlusion was defined as the absence of any residual filling of the target aneurysm, or a residual filling that was no deeper than 2 mm and did not exceed one-half of the neck diameter. This threshold was arbitrary chosen to mitigate interobserver variability in the evaluation of tiny aneurysm remnants, which do not require retreatment or rigorous surveillance and have minimal prognostic or therapeutic significance (12-14). True recanalization was defined as a verified increase in the size of the residual part at follow-up compared to the immediate postoperative result.

The safety endpoint was an occurrence of any adverse events related to the aneurysm or its treatment. This included: intraoperative technical complications, neurological complications, surgical morbidity and mortality.

The key procedural predictor assessed in this study was the treatment modality. In the FD group we also evaluated the presence or absence of contrast media retention, flow stagnation and partial thrombosis within the target aneurysm at the end of the procedure. In the EC group we documented whether there was a significant interstitial filling within the coiled aneurysm.

The anatomical predictors of the target aneurysm assessed in this study were:

• Aneurysm size (max dimension);
• Neck diameter;
• Aspect ratio (AR), size ratio (SR) and neck-to-dome ratio (NTDR);
• Technical angle;
• Exact location;
• Sac shape;
• Presence or absence of “unfavorable” neck anatomy;
• Presence or absence of incorporated side branches;
• Presence or absence of multiple aneurysms in the same or adjacent arterial segments;
• Rupture status.

The methods for evaluating the morphological indices of target aneurysms are illustrated in Figure 2. An “unfavorable” neck was defined by any of the following: a NTDR greater than 0.6, an absolute neck diameter exceeding 4 mm, or a neck diameter larger than the vessel diameter in the affected segment. The technical angle was determined as the angle formed between the aneurysm axis and a straight microcatheter track. The angle was deemed “unfavorable” if it exceeded 100°, indicating a potentially challenging catheterization of the target aneurysm.

Figure 2 Investigated morphological indices of the target aneurysms. a, technical angle; AR, aspect ratio; c, isocenter of the neck; D, vessel diameter; H, perpendicular height; L, aneurysm length; N, neck diameter; NTDR, neck-to-dome ratio; max, aneurysm maximum dimension (size); SR, size ratio; W, perpendicular width.

Statistical analysis was conducted using RStudio version 1.4 (Posit PBC, Boston, USA) with R language version 4.1.0 from CRAN project. The analysis utilized standard R tools including descriptive and comparative statistics, alongside specialized packages: TidyR (data cleaning and refinement), BlorR (regression analysis), pROC and ggplot2 (graphical representation).

Categorical variables were reported as absolute numbers (n) and percentages (%). The normality of numerical variables was assessed using the Shapiro-Wilk test. Given that all variables exhibited skewed distribution, they were reported as medians (Me) and interquartile ranges (IQRs).

Intergroup differences for categorical variables were evaluated using the Chi-squared test with Yates’ correction. For numerical variables, differences were assessed using the Mann-Whitney U test. Comparative statistics were reported with a 95% confidence interval (95% CI) and level of significance P=0.05, the P value was two-sided in all cases.

Predictor evaluation was carried out using univariable and multivariable logistic regression analyses. The effects were quantified through log-odds differences and estimated with odds ratios (ORs). For the regression analysis, the 95% CI and a significance level of P=0.05 was utilized. The comparison of predictive power of different regression models was assessed using analysis of variance (ANOVA) with a significance threshold of P=0.05.

The predictive value of regression models was further evaluated through receiver operating characteristic (ROC) curves and area under the curve (AUC) index. An AUC index of ≤0.6 was considered “poor”, 0.61–0.70 “acceptable”, 0.71–0.80 was determined as “good”, and ≥0.81 was deemed “excellent”.

Ethical declaration

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by local ethics committee of E.N. Meshalkin National Medical Research Center (NMRC) (No. 03-53-2015) and individual consent for this retrospective analysis was waived.

Results

Sample properties

The sample included 236 patients harboring a total of 258 target sIAs, representing 90.2% of all eligible cases (n=286) during the study period, all of which had a follow-up DSA available.

The median patients’ age was 52 years (IQR, 42–60 years), 202 patients were women (85.6%). The median sIA size was 6.3 mm (IQR, 5.3–7.7 mm), 60.8% of lesions (n=153) were less than 7 mm in size. The median neck diameter was 3.5 mm (IQR, 2.8–4.4 mm), 71.4% of aneurysms (n=183) exhibited unfavorable neck anatomy.

A total of 258 primary interventions were performed, of which 155 (60.1%) were EC, and 103 (39.9%) were FD. The baseline characteristics of patients, target aneurysms and treatments are summarized in Table 1.

The significant factors favoring the selection of FD over coiling included: ophthalmic location of the aneurysm (OR 3.35, 95% CI: 1.94–5.88, P<0.001), a side branch incorporated into the aneurysm (OR 8.8, 95% CI: 3.71–24.4, P<0.001), presence of multiple aneurysms in the affected arterial segment (OR 7.8, 95% CI: 3.77–18.76, P<0.001), increasing neck diameter (OR 1.54 per 1 unit increase, 95% CI: 1.25–1.94, P<0.001), and NTDR ≥0.6 (OR 5.26, 95% CI: 1.56–18.76, P=0.008).

Treatment outcomes

In the FD group, the rate of complete occlusion of the target aneurysm was significantly higher than in the mixed coiling group (OR 1.86, 95% CI: 1.08–3.28, P=0.02) and similar to that observed in the SAC subgroup (OR 0.95, 95% CI: 0.41–2.11, P=0.90). The incidence of intraoperative technical complications in the FD group was significantly lower compared to both the mixed-type EC group (OR 0.28, 95% CI: 0.11–0.63, P=0.003) and the stent-assisted EC subgroup (OR 0.23, 95% CI: 0.08–0.65, P=0.008).

Within the coiling subgroups, the rate of complete occlusion was significantly higher following the stent-assisted EC versus non-stent-assisted EC (OR 2.5, 95% CI: 1.19–5.67, P=0.01). Although there was a trend toward a lower rate of true recanalization in the stent-assisted EC subgroup, this difference did not reach statistical significance. (OR 0.46, 95% CI: 0.16–1.14, P=0.11). The rates of technical complications did not differ significantly between the two coiling subgroups (OR 1.26, 95% CI: 0.54–2.85, P=0.57). The occurrence of neurological complications, surgical morbidity and mortality was not significantly different between the groups and subgroups (Table 2).

The results of the subgroup analysis stratified by target aneurysm location are represented in Table 3. While flow diverters demonstrated higher rates of complete occlusion of the target aneurysm across all location subgroups, these differences did not reach statistical significance, likely due to the limited size of each subgroup. Notably, all location subgroups exhibited non-negligible rates of true recanalization following EC. Among posterior communicating artery aneurysms, the incidence of intraoperative technical adverse events was significantly lower with FD compared to coiling.

Procedural predictors

The use of FD compared to mixed-type EC was identified as a significant predictor against target aneurysm non-occlusion (OR 0.53, 95% CI: 0.3–0.92, P=0.02).

In the FD group, changes in intraneurysmal flow after device placement compared to the pre-treatment state indicated a trend against non-occlusion of the target aneurysm, however, this did not achieve statistical significance (OR 0.42, 95% CI: 0.14–1.09, P=0.11).

In the EC group, approximately one-half of all non-occlusion cases were attributed to true recanalization, while the remainder resulted from initial incomplete occlusion of the target aneurysm. Notably, significant interstitial filling of the coiled aneurysm at the end of the procedure was a significant predictor for both incomplete occlusion (OR 2.21, 95% CI: 1.07–4.6, P=0.03) and true recanalization (OR 3.53, 95% CI: 1.52–8.33, P=0.003) at the follow-up.

The use of SAC was identified as a significant predictor against non-occlusion of the target aneurysm when compared to non-SAC (OR 0.4, 95% CI: 0.18–0.84, P=0.01). In addition, there was a trend against true recanalization, however, this finding did not achieve statistical significance (OR 0.46, 95% CI: 0.16–1.14, P=0.11).

The use of FD was a significant predictor towards reducing the intraoperative technical adverse events in both the mixed-type EC group (OR 0.28, 95% CI: 0.11–0.62, P=0.04) and the subgroup of stent-assisted EC (OR 0.3, 95% CI: 0.07–0.88, P=0.03).

The incidence of neurological complications was 2% in the FD group, 4% in the mixed-type EC group, and 8% in the subgroup of stent-assisted EC. Overall, the morbidity and mortality rates were similar across the groups.

Anatomical predictors

The results of regression analyses with respect to the anatomical predictors are summarized in Tables 4,5.

In the FD group, univariable regression analysis identified the following factors significantly associated with incomplete occlusion of target aneurysms: increasing neck diameter (OR 1.42 per 1 mm increase, 95% CI: 1.02–2.04, P=0.03), unfavorable neck (OR 4.8, 95% CI: 1.27–31.5, P=0.04), a presence of incorporated side branch (OR 4.9, 95% CI: 1.88–13.4, P=0.001), and terminal location of the aneurysm (OR 10.5, 95% CI: 1.3–218, P=0.04).

Conversely, the following factors were identified as significant predictors towards the complete occlusion: increasing AR (OR 0.21 per 1 unit increase, 95% CI: 0.06–0.55, P=0.003), presence of multiple aneurysms in the same or adjacent arterial segments (OR 0.27, 95% CI: 0.07–0.8, P=0.02), and typical (elliptic or drop-like) shape of the target aneurysm sac (OR 0.27, 95% CI: 0.08–0.76, P=0.01).

The “positive” predictors (decreasing the odds of non-occlusion) and “negative” predictors (increasing the odds of non-occlusion) were subjected to multivariable analyses as “positive” and “negative” models, respectively. Multivariable analysis confirmed a significant association between all factors except terminal location, and their corresponding angiographic outcomes (see Table 3).

A predictive value of the full model, which incorporated all factors, was not significantly different from that of the reduced “positive” and “negative” models (P=0.32 and 0.15, respectively). The AUC indices for the “positive” and “negative” multivariable models were 0.78 (95% CI: 0.68–0.87) and 0.71 (95% CI: 0.60–0.82), respectively. The ROC curves for the aforementioned predictive models are shown in Figure 3A,3B.

Figure 3 The ROC-curves for multivariable regression models. (A) Flow diversion—“positive” model, (B) flow diversion—“negative” model, (C) endosaccular coiling—final model. CIs for AUC are reported in the text. AUC, area under the curve; CI, confidence interval; ROC, receiver operating characteristic.

In the EC group, univariable regression analysis revealed several predictors associated with incomplete occlusion of target aneurysms: increasing AR (OR 1.96 per 1 unit increase, 95% CI: 1.6–2.75, P=0.07), presence of multiple aneurysms in the same or adjacent arterial segments (OR 4.3, 95% CI: 1.14–20.6, P=0.04) and previous rupture of the target aneurysm (OR 3.9, 95% CI: 1.44–11.9, P=0.009). In contrast, the following predictors demonstrated a trend towards complete occlusion of target aneurysms: increasing neck diameter (OR 0.76, 95% CI: 0.55–1.03, P=0.09), and unfavorable technical angle of the target aneurysm (OR 0.23, 95% CI: 0.03–0.87, P=0.05).

According to the multivariable analysis, the following factors were significantly associated with incomplete occlusion of target aneurysm: unfavorable neck anatomy (OR 2.4, 95% CI: 1.05–5.74, P=0.04), increasing AR (OR 2.04, 95% CI: 1.12–3.88, P=0.02), multiple aneurysms (OR 4.71, 95% CI: 1.16–23.8, P=0.03), and previous rupture of the target aneurysm (OR 4.87, 95% CI: 1.16–12.1, P=0.01). Additionally, an unfavorable technical angle showed a trend towards complete occlusion of the target aneurysm (OR 0.24, 95% CI: 0.03–1.03, P=0.09). There was no significant difference in predictive power among the full model (which included all factors), the reduced model (including the technical angle) and the final model (excluding the technical angle), with P values of 0.25 and 0.11, respectively. The area AUC index for the final model was 0.67 (95% CI: 0.58–0.78). The ROC curve for the corresponding model is represented in Figure 3C.

Discussion

In our study, the most significant procedural predictor associated with total occlusion of the target aneurysm was the use of FD. In comparison to the mixed-type EC group, in the FD group we observed a remarkably higher rate of target aneurysm total occlusion (76% compared to 63%). On the contrary, the subgroup of SAC demonstrated a total occlusion rate similar to that of FD (also 76%).

In the EC group, the use of stent-assistance was identified as the most significant factor, increasing the likelihood of total occlusion (from 56% to 76%) while reducing the likelihood of true recanalization (from 32% to 15%) of the target aneurysms.

These findings corroborate with previously published studies. A meta-analysis by Fiorella et al. [2020] reported that small sIAs treated with FD achieved a pooled total occlusion rate of 75% at 12 months post-operatively (10). Meta-analyses by Phan et al. [2016] and Nabizadeh et al. [2024] indicated that total occlusion rates in non-stent-assisted EC typically do not exceed 60%, while stent-assisted EC can reach the total occlusion rates of 75–80% (6,15). These results are further supported by comparative studies. In mixed-type EC series, FD demonstrated significantly higher efficacy, achieving total occlusion rates of 70–80% compared to 50–60% for conventional coiling (16,17). Conversely, in studies where the control group consisted of SAC exclusively, both techniques exhibited similar efficacy, showing total occlusion rates of approximately 70–80% (18,19). The role of stents in enhancing aneurysm occlusion is well-documented. Not only do they increase coil packing density but also provide a modest flow-diverting effect and serve as scaffolds for endothelization (20).

Literature lacks consensus on whether changes in intraneurysmal flow immediately after FD placement can predict aneurysm occlusion at follow-up (21). In our series, the presence of intraoperative stasis or partial thrombosis demonstrated a modest trend towards complete occlusion of flow-diverted aneurysms.

Conversely, significant interstitial filling of the coiled aneurysm at the end of the procedure is a well-established risk factor for eventual non-occlusion (22). Accordingly, our study revealed that intraoperative interstitial filling was associated with both non-occlusion and true recanalization of coiled aneurysms at follow-up.

In our series, the use of FD not only demonstrated superior efficacy but also was associated with a lower rate of intraoperative technical adverse events compared to all types of coiling (less than 10% versus approximately 20%). This effect can be attributed to fever devices within the vessel lumen and no need to operate within the aneurysm sac, which collectively reduce the risk of manipulation-related issues. Additionally, the FD group exhibited the lowest rate of neurological complications when compared to both mixed-type EC and stent-assisted EC. Although these complications were rare and did not reach statistical significance between groups, even a slight increase in complication rates may be a major concern for previously asymptomatic patients.

Among the anatomical predictors, two factors were particularly noteworthy: the increasing AR of the target aneurysms, and the presence of multiple aneurysms within the same or adjacent arterial segments. In the FD group both factors were significant predictors favoring total occlusion of the aneurysm. In the EC group, vice versa, these same factors were significantly associated with incomplete occlusion of the target aneurysm.

The aneurysms with a high AR are associated with an increased risk of growth and rupture due to unfavorable internal hemodynamics, specifically blood retention, low volumetric flow, and low wall-shear stress, which contribute to the instability of the aneurysm wall (23). As a consequence, when treated with coils, such aneurysms may be more susceptible to delayed coil compaction and growth of the residual part (24). Conversely, these same features may enhance the hemodynamic effects of flow diverters, thereby improving their efficacy (25,26). We suggest that a similar hemodynamic mechanism underlies the increased probability of occlusion in aneurysms of typical shape treated with flow diverters, as observed in our study (26).

It remains unclear how the presence of multiple aneurysms can improve the efficacy of FD while at the same time diminishing the effectiveness of coiling. One potential explanation could be the technical challenges associated with a simultaneous coiling of multiple aneurysms. Another possible explanation may relate to local hemodynamics or unfavorable vessel anatomy associated with the formation of multiple aneurysms; however, these factors are not immediately evident and require further investigation (27,28).

In both groups, unfavorable neck anatomy was a significant predictor of target aneurysm non-occlusion. A poorly developed neck increases the technical complexity of coiling. Moreover, wide-necked lesions tend to have relatively high volumetric blood flow, which counteracts the effectiveness of flow diverters (29). Additionally, larger defects in the arterial wall are less susceptible to endothelization (30).

In the FD group, the presence of incorporated side branches was identified as another significant predictor of incomplete occlusion. An additional outflow pathway within the aneurysm increases the volumetric blood flow and flow gradient across the aneurysm neck, which inhibits thrombosis (31). A similar phenomenon may account for the increased likelihood of incomplete occlusion in terminal carotid aneurysms, which was also observed in our study. Such aneurysms, compared to those in other carotid locations are more likely to exhibit bifurcation-type hemodynamics, which is a well-established factor decreasing the efficacy of FD (32).

In the EC group, one more significant predictor of incomplete occlusion was a previous rupture of the target aneurysm. The rupture may trigger a biological response that alters the structure of the aneurysm wall and affects flow dynamics within the aneurysm, making it susceptible to reopening or regrowth after coiling. The association between a positive rupture history and an elevated risk of non-occlusion at follow-up is well-documented in the literature and corroborates the findings of our study (5).

The primary limitation of this study was the significant intergroup difference in the anatomical features of the target aneurysms (refer to Table 1). Lesions with complex and unfavorable anatomy were more likely to be treated with FD, while relatively simple cases were predominantly coiled. This discrepancy could lead to an underestimation of certain anatomical predictors in the EC group. To validate the identified predictors, a randomized or propensity-matched study is necessary, ensuring that groups have comparable anatomical features.

Additionally, this study has all limitations attributable to retrospective design and single-center enrollment. Another notable limitation was the relatively short follow-up period (median 9 months).

Conclusions

The use of FD was single the most significant predictor of total occlusion in target aneurysms. SAC emerged to be a significant predictor of total occlusion when compared to non-SAC.

In the FD group, an increasing AR of the target aneurysm and the presence of multiple aneurysms within the same or adjacent arterial segments were significantly associated with complete occlusion. Conversely, in the EC group these same two predictors were associated with incomplete occlusion of the target aneurysm. We consider these factors important when selecting the appropriate treatment modality for aneurysms that are amenable to both methods.

In the EC group, the presence of interstitial filling within the coiled aneurysm at the end of the procedure and a history of previous rupture of the target aneurysm were significant predictors of incomplete occlusion. In the FD group, a significant predictor for incomplete occlusion was the presence of an incorporated arterial branch. Additionally, in both groups, unfavorable neck anatomy was identified as a significant predictor of incomplete occlusion of the target aneurysm.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jni.amegroups.com/article/view/10.21037/jni-25-5/rc

Data Sharing Statement: Available at https://jni.amegroups.com/article/view/10.21037/jni-25-5/dss

Peer Review File: Available at https://jni.amegroups.com/article/view/10.21037/jni-25-5/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jni.amegroups.com/article/view/10.21037/jni-25-5/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.The study was approved by local ethics committee of E.N. Meshalkin National Medical Research Center (NMRC) (No. 03-53-2015) and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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