Ultrasound assessment of blood flow in branches of the external carotid artery as potential donors for microsurgical revascularisation of the central nervous system

Introduction

Vascular bypasses linking branches of the superficial temporal artery (STA) to cerebral arteries are a recognised method for treating selected cases of cerebral vascular conditions resulting in cerebral hypoperfusion (1,2). Indications for microsurgical revascularisation include moyamoya disease, which is the most common, as well as spontaneous arterial stenosis affecting the terminal segment of the internal carotid artery and arteries within the circle of Willis (3,4). The decision to perform microsurgical intervention is based on the failure of conservative therapy and recurrent ischaemic symptoms (1,2,4). In carefully selected patients, this approach may also be beneficial in cases of occlusions of the internal carotid artery, middle cerebral artery (MCA), or anterior cerebral artery and their branches, caused by factors such as atherosclerosis or trauma. Recent findings show favorable, long-term outcomes of microsurgical treatment for internal carotid artery (ICA) or MCA occlusion, with effects observed after more than 5 years—indicating an advantage over pharmacological treatment alone (5-8). Typically, microsurgical revascularization is considered after conservative options have been exhausted (9). The primary cause of symptoms in these cases is reduced blood flow to the brain tissue supplied by the affected vessel. In an adult brain, about 57 mL of blood passes through every 100 g of tissue each minute, totaling roughly 800 mL for an average 1,400 g brain (10). Each internal carotid artery supplies approximately 280 mL of blood per minute, meeting the needs of its respective hemisphere (11). As blood flow declines with steno-occlusive disease progression, collateral vessels initially compensate by increasing flow, forming alternative pathways. The severity of clinical symptoms depends on the effectiveness of these collateral routes. Inadequate compensation can lead to serious consequences (12). Symptoms mainly arise from reduced blood flow to brain tissue supplied by the affected vessel, which can develop gradually, as in moyamoya disease or syndrome, or result from atherosclerotic changes. A sudden blockage, due to vessel dissection or embolic material, often causes a significant ischaemic stroke.

Many reports have focused on the effects of microsurgical revascularisation treatment: the maturation process of vascular grafts over time is evaluated (13,14), as well as patients’ cognitive functions and daily activities during treatment (15). Preoperative assessment of patients scheduled for microsurgical procedures often does not include ultrasound examination of donor vessels. Instead, classical angiography and assessments using computed tomography (CT) or magnetic resonance imaging (MRI) are employed to evaluate potential donor vessels. However, these methods do not allow for the evaluation of blood flow within the assessed vessels, meaning the capacity of these vessels to supply cerebral circulation remains unknown. Understanding individual variability in blood supply capacity, along with the impact of potential cardiovascular risk factors, could improve the process of selecting a suitable donor vessel in relation to the patient’s own vascular bed. The efficiency of a shunt in a bypass procedure depends on the timeframe after surgery and conditions (mainly the rate of hypoperfusion before surgery). Its flow mainly reflects the haemodynamic demand of the connected brain segment. An additional key factor is how this flow changes over time due to the reorganization of the brain’s haemodynamic relationships. This leads to variations in the flow measurements within the shunt as time passes after the procedure (13,16).

So far, few attempts have been made to preoperatively evaluate the potential to support or replace the patient’s inadequate circulation with a bypass from another vessel. Therefore, it is important to assess the suitability of the STA and its branches for this purpose.

Objective

This study aimed to evaluate, using Doppler ultrasound, the flow parameters and dimensions of the temporal arteries and their small terminal main branches, the frontal and parietal arteries. We sought to assess the potential of these vessels to form an effective collateral circulation route through bypass techniques in specific ischaemic cerebrovascular diseases. The analysis focused on the Polish population, which had not been previously studied in this context. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2696/rc).

Methods

Patients

The subjects were recruited as volunteers from patients of the Neurology Department with Stroke Unit at Lower Silesia Specialist Hospital of T. Marciniak-EMC in Wroclaw, who were admitted for non-vascular reasons, as well as from patients at the PhysioTeam Clinic in Wroclaw, also diagnosed with non-vascular causes. The participants were additionally selected to ensure a representative sample in each age decade, divided by gender.

Demographic data, including risk factors for cardiovascular disease (such as hypertension, diabetes, and smoking) and anthropometric measurements (height and weight), were collected and are shown in Table 1. Detailed demographic information, illustrating the distribution of patients across each age decade within the study, is displayed in Table 2.

The study was conducted in accordance with the Declaration of and its subsequent amendments. The study was approved by the Bioethics Committee at the Lower Silesian Medical Chamber (No. 10/BOBD/2024), and informed consent was taken from all the patients. The other participating hospital was informed of and agreed to this study.

Ultrasound examination technique

STAs, along with their frontal branches (FBs) and parietal branches (PBs), were examined using Doppler ultrasound. To exclude proximal vascular pathology that could influence flow in the examined vessels, the internal and external carotid arteries and vertebral arteries were also assessed. The measurement sites for the STA, FB, and PB are shown in Figure 1. The STA was examined distal to the transverse facial artery, zygomatic-orbital artery, and middle temporal artery. Measurements were taken at or just above the tragus of the ear, with the artery’s course approximately 1 cm anterior. The FB and PB were examined roughly 10–25 mm above the STA bifurcation, depending on anatomical conditions. In each case, the aim was to obtain the most favourable angle of insonation α for the vessel’s course in each patient. The Doppler gate was centred on the examined artery, with its size adjusted to match the artery’s diameter. In most cases, a 1-mm Doppler gate was used for the STA trunk. The insonation angle was kept below 60° in all cases. We made an effort to minimise the impact of ultrasound transducer pressure on small vessels. Assessments in these vessels were conducted after locating a straight segment in the suitable part of the vessel and then reducing the pressure until artifacts emerged that hindered calculations. Systemic blood pressure was also evaluated as a possible factor influencing the outcomes. For hospitalised patients, it was measured twice daily and remained within the normal range on the examination day. At the PhysioTeam Clinic, blood pressure was measured during a doctor’s visit and was normal in all instances. Flow parameters measured in individual vessels included peak systolic velocity (PSV), end-diastolic velocity (EDV), mean velocity (MnV), and, for the temporal artery trunk, minute flow. The examination was conducted using an Aloka Prosound Alpha 6 device with a linear transducer operating at suitable frequencies of 4–13 MHz. Measurements were made using the built-in software of the ultrasound device.

Figure 1 Measurement locations for individual vessels (Henry Gray; Gray’s Anatomy, 20th edition; 1918; page 554, Figure 508—the arteries of the face and scalp, Public Domain). Modified by authors. FB, frontal branch; PB, parietal branch; STA, superficial temporal artery.

Inclusion and exclusion criteria

The study involved adults (aged 18 years or older at the time) who had not previously been diagnosed with any vascular disease, particularly atherosclerosis in any vascular bed. Participants provided informed consent to take part in the project.

According to the study protocol, individuals in whom it was not possible to visualise all the arteries included in the study were excluded. Specifically, in two cases, the PB of the right temporal artery could not be visualised, and in four cases, on the left. Individuals with newly discovered haemodynamically significant stenosis of any extracranial artery during this study were also excluded; two volunteers were referred to a vascular surgeon for consultation due to asymptomatic stenosis of the internal carotid artery. Six patients were referred to a cardiology outpatient clinic for arrhythmia, and eleven patients to an endocrinology clinic due to newly discovered focal thyroid lesions. Detailed inclusion and exclusion criteria are presented in Table 3 and Figure 2.

Figure 2 Flow chart illustrating the process of selecting volunteers for the study.

Statistical analysis

Statistical tests were performed at a significance level of α=0.05. Comparisons between patient groups used Wilcoxon tests (for dependent samples), Student’s t-tests, Mann-Whitney tests, and Kolmogorov-Smirnov tests (for independent samples). The Shapiro-Wilk test checked for normal distribution. Pearson’s correlation coefficient was employed to evaluate correlations.

The distribution was fitted to the data using the maximum likelihood method across the following probability distributions: Birnbaum-Saunders, Burr, Exponential, Extreme value, Gamma, Generalised Extreme Value (GEV), Pareto, Half-Normal, Inverse Gaussian, Logistic, Log-logistic, Log-normal, Nakagami, Normal, Rayleigh, Rice, Stable, Weibull, and Student’s t.

The analyses were performed using MATLAB software, version R2024b, on Windows 10 Pro 64-bit.

Results

The study involved 157 participants who met the exclusion criteria, including 78 women aged 18–89 years, all of whom were Caucasian. The analysis examined the distributions of artery diameters in relation to age and gender. The measurements of the left temporal artery ranged from 0.7 to 2.3 mm, with standard deviation (SD) of 0.359 while the FB and PB ranged from 0.4 to 1.5 mm (SD for FB was 0.178 and for PB 0.158). The measurements of the right temporal artery ranged from 0.8 to 2.4 mm (SD was 0.246), with the FB also ranging from 0.4 to 1.5 mm (SD was 0.18), and the PB from 0.3 to 1.3 mm (SD was 0.184). The diameter distribution of the left temporal artery trunk follows a Student’s t-distribution; the FB and PB follow a Burr distribution. On the right side, the temporal artery trunk follows a Gamma distribution, the FB follows a GEV distribution, and the PB follows a Burr distribution, as shown in Figure 3. The diameters of all arteries differ significantly between females and males, warranting a gender-specific analysis. Detailed values are presented in Table 4. Box plots comparing artery diameters for women and men, along with density plots of fitted theoretical distributions, are provided in Figures 4,5. Flow values in the temporal arteries were also evaluated, with distributions in relation to age. In women, flows in both temporal arteries follow a GEV distribution, while in men, they follow a Stable distribution. Detailed box plots, histograms, and distribution comparisons are shown in Figure 6.

Figure 3 Histograms and theoretical densities of fitted distribution for left and right STA and its branches. FB, frontal branch; LSTA, left superficial temporal artery; PB, parietal branch; RSTA, right superficial temporal artery; STA, superficial temporal artery; Theo. dist., theoretical distribution.

Figure 4 Graphs comparing the diameters of each of the tested vessels for women and men, and density graphs of theoretical distributions—left side. FB, frontal branch; LSTA, left superficial temporal artery; PB, parietal branch; Theo. dist., theoretical distribution.

Figure 5 Graphs comparing the diameters of each of the tested vessels for women and men, and density graphs of theoretical distributions—right side. FB, frontal branch; PB, parietal branch; RSTA, right superficial temporal artery.

Figure 6 Box plots, histograms, fitted distributions, and theoretical density comparisons. GEV, generalised extreme value; LSTA, left superficial temporal artery; RSTA, right superficial temporal artery.

The vessel diameters for each group, female and male, were compared across different age brackets as detailed in Table 2. Box plots showing these vessel diameters for each age group, including the mean and separated by gender, are presented in Figure 7.

Figure 7 Box plots of vessel diameters for each age group, including mean value. FB, frontal branch; LSTA, left superficial temporal artery; PB, parietal branch; RSTA, right superficial temporal artery.

We examined the relationships between weight and carotid artery diameter, as well as height and carotid artery diameter, within the study group. Separate linear regression models were created for each side. The findings indicated a trend: as body weight and height increased, so did the diameter of the carotid artery. These results are shown in Figure 8.

Figure 8 Linear regression models for height, weight, and temporal artery diameter. LSTA, left superficial temporal artery; RSTA, right superficial temporal artery.

Blood flow in the temporal arteries was evaluated. On both sides, the distribution of flow values within the population was characterised by a Stable distribution. Normalised histograms for flows in the left and right temporal arteries in the study population, along with the theoretical density of the selected distribution, comparisons of empirical distributions, and colour-quantile plots, are shown in Figure 9. No differences were observed between the left and right sides in the study population; detailed values are provided in Table 5.

Figure 9 Normalised histograms for LSTA and RSTA flows in the studied population with the theoretical density of the fitted distribution, comparisons of empirical distribution functions, and quantile plots. LSTA, left superficial temporal artery; RSTA, right superficial temporal artery; Theo. dist., theoretical distribution.

Blood flow in the left temporal artery showed no statistically significant difference between women and men (P value =0.051, slightly above the α=0.05 cutoff). In contrast, a significant sex difference was observed in the right temporal artery. Detailed data can be found in Table 5.

Pearson’s correlation coefficient analysis showed no significant relationships between the diameters of the examined arteries—the STA, FB, and parietal artery—on both the left and right sides.

The influence of risk factors such as diseases (arterial hypertension or diabetes) and adverse health behaviours (nicotine addiction) on the diameters and flow values in the studied vessels was assessed. However, no statistically significant effects were found for any of these factors.

Discussion

The preferred methods typically for the interventional treatment of acute cerebral ischaemia are currently fibrinolytic and endovascular approaches. Intravenous medications that activate the conversion of plasminogen and endovascular procedures involving the direct removal of embolic material from the vessel are used (17). Advances in techniques, tools, and postoperative care protocols have resulted in good outcomes, characterised by high recanalisation rates and clinical effects, as evaluated with the Rankin scale (18). Despite this, the procedures mentioned above are not entirely effective in all clinical situations. Therefore, there is growing interest in the emergent and elective use of bypass as a method for treating ischaemia (2,19). The technical feasibility of performing bypass, the safety of the procedure, and its effectiveness in carefully selected patients have been demonstrated (20-22). It is crucial to remember that the haemodynamic conditions and clinical status of the brain differ between acute and chronic ischaemia. The urgency of the procedure is particularly important. In urgent cases of acute ischaemia, the operation focuses on rescuing the penumbra. In chronic cases, treatment focuses on alleviating hypoperfusion of the selected brain segment (2,4,5). In chronic ischaemia, particularly caused by gradually increasing stenosis (especially in the case of anatomical variables), endovascular methods may not be effective. Considering the exhaustion of conservative treatment options [best medical treatment (BMT)] (23), the next therapeutic choice is surgical indirect or direct revascularisation. As a prime example, indirect revascularisation has proven effective in decreasing the risk of ischaemic or haemorrhagic events in the course of moyamoya disease (24), as well as being a more haemodynamically effective procedure, direct vascular bypass (10). Bypass surgery can serve as a third-line rescue option when pharmacological therapy, thrombolysis, and mechanical thrombectomy are unsuccessful in treating acute ischaemia. A recent study showed significantly improved outcomes in patients for whom this procedure was feasible (25).

A comprehensive preoperative assessment of the patient involves several additional tests. Digital subtraction angiography is the gold standard for evaluating the anatomy of cerebral and pre-cerebral vessels. Perfusion imaging (CT or MRI) helps identify areas that might be at risk of ischaemia, though the criteria for its use are still under discussion. In research protocols, it serves as a supporting factor for including or excluding the method in cases of very extensive stroke (5). Neuropsychological assessment aims to pinpoint key functional areas where deficits might occur (26). Despite extensive preoperative diagnostics—including identifying regions requiring revascularisation and assessing the technical feasibility of the procedure (by imaging suitably located vessels that serve as donors for the planned grafts)—uncertainties remain regarding the vessels’ capacity to deliver blood and, therefore, their ability to support or replace the patient’s own cerebral circulation. These uncertainties highlight the need to develop a method for assessing flow in potential donor vessels that is as non-invasive and repeatable as possible.

Our study provides a solid basis for further research into the potential use of branches of the STA as donors to support or restore cerebral circulation across various cases and conditions. In the study, we demonstrated differences in both the diameters of the examined arteries and the assessed flow parameters between female and male populations. The larger vessel diameter and blood flow volume suggest a greater supply capacity in the male population. This indicates a potential for improved long-term treatment outcomes in this group. Similar disparities have been reported for coronary arteries (27), internal carotid arteries, vertebral arteries (28), and femoral arteries (29). Importantly, we did not observe any significant differences in the parameters across age groups. Our data indicate that revascularisation potential is equally favourable in both younger and older patients. This has important clinical implications, given the wide range of conditions in which bypass surgery may be considered a therapeutic option.

Overall, no statistically significant differences were found between the left and right vessels across patient groups. However, some individual patients showed very substantial differences. This emphasises the importance of assessing both vessels in each patient. Asymmetry in paired arteries has been documented across various vascular regions, including cerebral and limb arteries (30). Individual side dominance may result from unique genetic/developmental factors; however, this does not generalise statistically.

We observed a gradual increase in mean arterial sizes and blood flow volume with rising body weight and growth in both female and male groups. However, the estimation curve showed a very slight slope; the increase in vessel diameter on the Y-axis was minor compared to the rise in body weight and height (shown on the X-axis). A detailed analysis revealed minimal fluctuations in the studied parameters, despite notable differences in height and body weight (height of 160 cm corresponds to a vessel diameter of approximately 1.4 mm in the linear regression model, while 180 cm slightly exceeds 1.5 mm; patients weighing 60 kg have an STA diameter of about 1.5 mm, and those weighing 120 kg approximately 1.6 mm). Similar findings have been previously reported for coronary arteries (19), with no significant differences in artery diameters related to body weight, height, or their derived parameters. Flow rates in arteries of under one millimeter scale, such as branches of the STA, are therefore below 10 mL/min. This contrasts with bypass studies that have shown the STA graft can provide flow rates of up to 100 mL/min (10,16).

We also examined whether it is possible to test the potential of donor vessels by focusing on those that precede them and are more accessible. In our study, we measured the diameters and blood flow volumes of the external carotid arteries. We found no significant correlations between the diameters and blood flow rates of the terminal branches compared to the trunk of the temporal artery, as well as between external carotid artery (ECA) and STA. This suggests that directly assessing the vessel intended as a graft donor is crucial in each revascularisation case. Relying on indirect measures, such as the diameters or flows of preceding vessels (e.g., ECA or STA for planning a graft from the PB), appears insufficient for a comprehensive evaluation.

Other studies have also noted differences in the calculated vessel diameter for the STA and its branches. The referenced meta-analysis compared pathomorphological measurements with radiological ones obtained via CT angiography. In these radiological studies, the measurements of the STA were slightly higher, while those for the FB and PB were slightly lower. Details are shown in Table 6 (31). Results of our analysis differ slightly from those mentioned above, likely due to different examination methods.

Potential risk factors for cardiovascular disease (such as hypertension, diabetes, or nicotine addiction) did not significantly influence the measured parameters. However, this result is limited by the small size of groups with risk factors and their uneven distribution, such as the higher prevalence of diabetes among older patients. The study did not distinguish between types of diabetes, duration of the disease, or treatments. Similarly, hypertensive patients were not categorised based on disease control, medication, or duration. The effect of comorbidities on flow parameters is further complicated by the presence of multiple factors in some individuals. Participants with a history of cardiovascular disease or those diagnosed during the study were excluded. Future research with larger populations and consideration of these variables is likely to generate valuable insights.

Despite the study’s limitations, especially in assessing the impact of comorbidities on flow parameters, the results are encouraging. We demonstrated that it is technically feasible to examine STAs and their branches in nearly all volunteers included in the study. There were no major difficulties in imaging the vessels related to their course. After visualising each vessel, it was possible to identify a segment suitable for Doppler flow assessment in the target area. We confirmed our initial assumptions about the need for separate evaluation of female and male populations, as well as the minimal influence of body weight and height on vessel diameters. A key clinical finding is the lack of a significant correlation between flow in the examined vessels and that in the preceding vessels. We hope that comparing the results from the healthy population with data from patients undergoing surgical treatment will improve our understanding of the bypass maturation process, assist in identifying potential favourable and unfavourable prognostic factors, and help predict the haemodynamic outcomes of therapy in specific patients.

Limitations of the study

The study has some limitations. The anatomy of the FB and PB of the temporal artery displays many variants and tortuosity, which often complicates locating straight vessel segments free of kinks, thereby affecting accurate flow velocity measurements. Individual differences in the presence of other branches—such as the transverse facial artery, zygomatic-orbital artery, and middle temporal artery—before they divide into terminal branches create a risk of missing these vessels and misestimating the measurement site for the STA. Variations in the thickness and echogenicity of the subcutaneous tissue along the vessels can hinder diameter measurements. Additionally, scalp hair at the measurement site, especially over the PB, can obstruct ultrasound beam penetration due to multiple boundaries between media with different densities, such as hair and air. We initially considered using a transducer with higher frequencies, which could improve imaging of shallow tissues. However, we abandoned this idea as we also needed to examine deeper arteries. The inclusion of patients with visible cardiovascular disease was considered, but we decided against it. Instead, we recruited only healthy patients for this study and excluded those with haemodynamically significant vascular stenosis.

Furthermore, the study concentrated solely on adult patients. We chose not to include paediatric patients because their rapid growth results in increases in vessel diameter and blood volume per unit time. This would necessitate dividing the paediatric population into numerous age subgroups for separate assessment. Additionally, the non-linear growth and maturation process, along with the variability in puberty onset, make age-based assessments in children difficult.

We have not tested patients for lipid metabolism or other laboratory parameters of potential vascular failure markers. Since our study was non-invasive, examining biochemical parameters simultaneously offers a promising avenue for future research. Larger study groups could enhance statistical power and uncover stronger correlations.

The calculation method may be less precise than quantitative MRI imaging in individual cases. However, one of our goals was to evaluate the potential of a simpler, more easily repeatable technique that could also be performed at the bedside.

We also identified a problem with a pressure device impacting blood flow in small vessels. This problem was observed during the exam as a reduction in EDV. Taking multiple measurements and averaging them might improve accuracy. In our study, we did not repeat measurements unless needed.

Conclusions

Our study showed that it is feasible to measure the course, diameter, and flow parameters of the STA and its terminal branches (frontal and parietal) in most cases. Ultrasound exams can be done at the bedside, offering a good balance between accuracy and practicality. We identified potentially significant differences between sexes, emphasising the need to analyse each population separately and establish specific standards. The findings are presented with graphs and curves illustrating the distribution of diameters and flows within the population. These results could assist in long-term predictions of revascularisation potential via vascular bypasses from the grafted vessel, paving the way for future research. This study might also help identify patients who, due to STA anatomy, may need more complex procedures, such as internal maxillary artery (IMAx) surgery, rather than the classical STA-MCA bypass.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2696/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2696/dss

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2696/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 the Bioethics Committee at the Lower Silesian Medical Chamber (No. 10/BOBD/2024), and informed consent was taken from all the patients. The other participating hospital was informed of and agreed to this study.

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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