Perioperative alteration of posterior tibial artery perfusion by contrast-enhanced ultrasound in patients with peripheral artery disease after endovascular therapy

Introduction

Peripheral artery disease (PAD) is a prevalent cardiovascular disease, affecting as many as 236 million people worldwide (1). It is characterized by chronic insufficient blood supply to the lower limbs, leading to intermittent claudication and critical limb ischemia (2,3). Revascularization, either through endovascular therapy (EVT) or conventional open surgery, remains a priority for patients with symptomatic and life-limiting PAD, potentially preventing limb-threatening complications and mortality (2,3). Due to its minimally invasive nature and lower complication rates, EVT is recommended as a first-line treatment for PAD, particularly in patients with significant comorbidities or a high surgical risk (4). However, restenosis rates following EVT can reach 40–60% within 12 months post-procedure (5), highlighting the importance of timely postoperative evaluation and long-term follow-up in optimizing patient outcomes.

Peak systolic velocity (PSV), measured by Doppler ultrasound (DUS), is a crucial parameter for evaluating the efficacy of EVT and long-term follow-up (6,7). PSV of the tibial artery is effectively used for diagnostic purposes and perioperative hemodynamic assessment following above-knee EVT in patients with PAD (6,7). However, PSV measurement requires high technical proficiency and can vary significantly between operators, potentially compromising its accuracy and repeatability (8). Moreover, PSV primarily evaluates intravascular hemodynamics but does not directly provide information on luminal perfusion, which is critical for assessing clinical outcomes. Further, PSV often exhibits delayed and potentially misleading responses during the early post-EVT period due to confounding factors such as edema or vasoconstriction, which undermine its reliability in immediate postoperative assessment (9,10). Therefore, a method that enables the direct assessment and quantification of vascular perfusion is needed to improve PAD management.

Contrast-enhanced ultrasound (CEUS) has gained broad diagnostic applicability in both macrovascular and microvascular imaging, and can be used to quantitatively evaluate intraluminal perfusion and irregularities, and end-organ perfusion for various vascular pathologies (11-17). The CEUS examination is fast and allows repeated measurements from the stored imaging. The microbubble contrast agent (e.g., SonoVue) has a favorable safety profile, and is neither nephrotoxic nor radioactive (11-17). To date, research on both the alteration and potential clinical utility of the luminal CEUS perfusion parameters of the posterior tibial artery (PTA) appears to be limited. Therefore, this study aimed to examine alterations in the PTA CEUS perfusion parameters in PAD patients following above-knee EVT, and to investigate the feasibility of using such parameters to monitor EVT-induced hemodynamic changes. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-426/rc).

Methods

Patient enrollment and ethics statement

This retrospective single-center study was conducted between January 2020 and February 2022. Patients were included in the study if they met the following inclusion criteria: (I) were symptomatic of PAD according to the guidelines on the diagnosis and treatment of PAD (18); (II) had undergone above-knee EVT for de novo lesions with a downstream outflow of the PTA; (III) had undergone pre- and post-EVT CEUS of the PTA within 14 days; and (IV) had complete CEUS perfusion parameters and patient clinical information (including information on demographics, comorbidities, and clinical symptoms) without any deletions. Patients were excluded from the study if they had not undergone both preoperative and postoperative CEUS examinations (n=66), had incomplete CEUS perfusion parameters (n=17), had used medications affecting perfusion (n=11), or had not successfully undergone EVT (n=0). Ultimately, a total of 43 consecutive patients with PAD (in 43 limbs) were included in the study. For further details, refer to the study flow chart (Figure 1).

Figure 1 Study flow chart. CEUS, contrast-enhanced ultrasound; PAD, peripheral artery disease.

This study was approved by the Ethics Committee Institutional Review Board of Huadong Hospital, affiliated with Fudan University (Approval No. 2022K171). Written informed consent was obtained from all the patients for the procedures (EVT and CEUS) and for data collection. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

CEUS examination and CEUS perfusion parameter collection

The Aplio500 ultrasound system (Toshiba, Japan) with a 6–12-MHz wide-band linear transducer (7L-probe) was used in this study. The instrument parameters (transmission frequency: 6 MHz, mechanical index: 0.08, acoustic output: 5%, depth: 4 cm, single focus zone at 2.75 cm, gain: 36 dB, and unit: mm) were applied consistently across all patients (12-14). All the CEUS examinations were performed by one certified vascular sonographer with more than 15 years of experience.

A stepwise protocol for the CEUS examination was employed (12,13,15). Specifically, after a 10-minute rest, all patients were positioned supine with the targeted lower limb fully exposed, slightly abducted, and externally rotated. DUS was performed in transverse orientation to assess the patency and inner diameter of the PTA. PSV was then measured in longitudinal orientation, and a 3-cm segment of the distal third of the PTA was selected as the region of interest (ROI) for CEUS. The system was then switched to CEUS mode. SonoVue (59 mg/ampoule, Bracco, Italy) (12,15), a suspension of phospholipid-stabilized sulfur hexafluoride microbubbles, was used as the contrast agent in this study. According to the manufacturer’s instructions, 59 mg of SonoVue was reconstituted with 5 mL of aqueous solution (12,15). Half of the reconstituted suspension (2.5 mL) was administered as a bolus injection via an antecubital vein, followed by a 5.0 mL saline flush. The built-in timer was activated simultaneously for imaging acquisition. The probe was fixed in place for 3 min, during which dynamic images were continuously and automatically acquired and stored on the instrument’s hard disk.

Medical digital image software (SonoLiver, Tomtac, Japan) was used for the offline analysis. A circular ROI (radius ≈1 mm) (12,13) was generated at the examined arterial segment. A time-intensity curve (TIC) was plotted to quantify CEUS perfusion parameters, including peak intensity (PI), time to peak (TTP), mean transit time (MTT), slope, area, area wash in (AWI), and area wash out (AWO) (12,13). PI, area, AWI, and AWO reflected the blood flow volume, while TTP, MTT, and slope reflected the blood flow velocity (Table 1) (10). A schematic diagram depicting the perfusion parameters is shown in Figure 2. To minimize artifacts, three distinct ROIs were obtained, and the mean of each parameter was calculated. The CEUS analysis was performed independently by two experienced radiologists (each with more than 10 years of experience in vascular ultrasound and more than 5 years of experience in CEUS) who were blinded to the EVT procedure and outcomes.

Figure 2 Schematic diagram of perfusion parameters. AWI, area wash in; AWO, area wash out; MTT, mean transit time; PI, peak intensity; S, slope; TTP, time to peak.

EVT procedure

During the EVT procedure, lower limb arterial angiography was completed for angiographic evaluation. The vessels were primarily prepared by plain ordinary balloon dilation by Ultraverse (3–6 mm in diameter, 60–220 mm in length, Bard, America), with or without percutaneous mechanical thrombectomy by the Rotarex system (6F, 110 cm in length, Straub Medical, Switzerland). Dilation with a drug-coated balloon (4–6 mm in diameter, 80–300 mm in length, Acortec, China) was occasionally performed. A provisional stenting protocol was subsequently used to treat above-knee superficial arterial and popliteal arterial lesions in cases of flow-limiting dissection, a recoil of >30.0%, or residual stenosis. A primary stenting protocol was applied for those iliac arterial lesions. The stents were chosen at the discretion of vascular surgeons. A vascular closure device (Perclose ProGlide, Abbott, California) was deployed for entry site closure after the completion of the procedure.

Statistical analysis

SPSS (version 25.0) software (IBM Corp., Armonk, NY, USA) and R software (version 2024.12.0.0; R Foundation for Statistical Computing, Vienna, Austria) were used to perform the statistical analysis. The Kolmogorov-Smirnov test was used to assess the normality of the continuous data. The normally distributed continuous data are presented as the mean ± standard deviation, and were compared between groups using paired samples t-tests. The non-normally distributed continuous data are presented as the interquartile range, and were compared using the Wilcoxon rank-sum test. The categorical data are expressed as the count (n) and percentage (%). The reliability and agreement of the perfusion parameters measured by the two physicians were assessed by Bland-Altman analysis. The correlation between the CEUS perfusion parameters and PSV was evaluated by Spearman correlation analysis. A P value <0.05 was considered statistically significant.

Results

Patient characteristics

A total of 43 consecutive patients (33 males; age range, 56–92 years; mean age: 72.56±10.19 years) with 43 affected limbs were included in the study. All the patients underwent above-knee EVT, and pre- and post-EVT CEUS examinations. Table 2 sets out the patient characteristics. In terms of comorbidities, 17 (39.5%) patients had diabetes mellitus (DM), 13 (30.2%) had hypertension, and 10 (23.3%) had chronic kidney disease (CKD). Additionally, 8 (18.6%) patients were current/former smokers. Other comorbidities included cardiac disease (7, 16.3%), cerebrovascular disease (5, 11.6%), and hypercholesterolemia (1, 2.3%). Five patients (11.6%) had prior lower extremity arterial revascularization. According to the Rutherford classification, the cohort comprised 19 patients (44.2%) with category 3 PAD (severe intermittent claudication), 23 patients (53.5%) with category 4 PAD (rest pain), and one patient (2.3%) with category 5 PAD (minor tissue loss).

Consistency and reliability analysis of the CEUS perfusion parameters

Two radiologists independently evaluated the CEUS perfusion parameters of the 43 lower limbs pre- and post-EVT. No significant differences were found between the measurements obtained by the two radiologists (P>0.05). The Bland-Altman analysis revealed that the differences between the two radiologists were randomly distributed around the mean difference, showing no significant trend or correlation with the magnitude of the measurements (Figure 3).

Figure 3 Bland-Altman analysis of perfusion parameters. In all plots, the central line represents the mean difference (bias), and the upper and lower dashed lines represent the 95% limits of agreement. AWI, area wash in; AWO, area wash out; EVT, endovascular therapy; MTT, mean transit time; PI, peak intensity; TTP, time to peak.

Perioperative alteration of PSV and the CEUS perfusion parameters

As shown in Table 3, PSV significantly increased from 26.27±21.03 to 49.01±25.79 cm/s after EVT (P<0.001), the TTP was significantly shorter post-EVT (7.01±3.12 s) than pre-EVT (11.74±8.20 s, P<0.001), and the MTT decreased from 23.00±11.51 to 18.16±7.87 s (P=0.002). The slope was steeper post-EVT compared to pre-EVT (32.56±54.18 vs. 19.01±23.04 ×10⁻⁵ AU/s, P=0.025). PI, area, AWI, and AWO did not differ significantly pre- and post-EVT (P=0.116, P=0.530, P=0.847, and P=0.469, respectively). Figure 4 displays representative images of perioperative changes in PSV and the CEUS perfusion parameters. Figure 5 shows box-and-whisker plots of these parameters.

Figure 4 A 71-year-old female patient underwent CEUS of the right PTA. (A) Pre-EVT PSV: 11.0 cm/s. (B) Pre-EVT CEUS and TIC, showing heterogeneous hyperenhancement (as indicated by the white arrow). Perfusion parameters: PI: 38.9×10⁻⁵ AU; TTP: 20.3 s; MTT: 15.3 s; slope: 1.9×10⁻⁵ AU/s; area: 1,378.6×10⁻⁵ AU·s. (C) Post-EVT PSV: 36.6 cm/s. (D) Post-EVT CEUS and TIC, showing significant enhancement (as indicated by the white arrow). Perfusion parameters: PI: 960.1×10⁻⁵ AU; TTP: 4.7 s; MTT: 14.5 s; slope: 342.6×10⁻⁵ AU/s; area: 40,380.9×10⁻⁵ AU·s. CEUS, contrast-enhanced ultrasound; EVT, endovascular therapy; MTT, mean transit time; PI, peak intensity; PSV, peak systolic velocity; PTA, posterior tibial artery; TIC, time-intensity curve; TTP, time to peak.

Figure 5 Box-and-whisker plots of hemodynamic parameters before and after EVT. AWI, area wash in; AWO, area wash out; EVT, endovascular therapy; MTT, mean transit time; PI, peak intensity; PSV, peak systolic velocity; TTP, time to peak.

Correlation between PSV and the CEUS perfusion parameters

As detailed in Table 4, PI (r_s=0.335), TTP (r_s=−0.357), MTT (r_s=−0.405), Slope (r_s=0.371), Area (r_s=0.279), AWI (r_s=0.249), and AWO (r_s=0.278) all exhibited statistically significant (P<0.05) but weak correlations with PSV.

Discussion

Previous studies (6,7) have shown that lower extremity vascular PSV can serve as an indicator of PAD severity and exhibits significant improvement post-EVT, suggesting its potential utility in assessing downstream hemodynamic changes. Consistent with these findings, the PSV of the PTA also increased significantly post-EVT in this study. However, this diagnostic approach is inherently limited by its operator-dependent nature, resulting in substantial interobserver variability and potential measurement inaccuracies (8,19). Further, it only provides static blood flow measurements, which fail to capture the dynamic nature of vascular perfusion (9). Conversely, CEUS uses a contrast agent to provide dynamic evaluations of both blood volume and blood flow velocity, offering a more comprehensive and accurate assessment of vascular conditions across multiple levels (20,21). At the macrovascular level, it objectively assesses luminal patency by tracking the filling of the microbubbles. At the microvascular level, perfusion parameters are quantified to reflect the capillary flow rate and relative blood volume. Further, at the tissue perfusion level, the diffusion kinetics and washout patterns of the microbubbles into the periarterial soft tissues serve as a functional indicator of distal nutrient delivery. Given that CEUS and PSV capture fundamentally different aspects of hemodynamics, we further explored their correlation. The observed weak correlations (maximum |r_s|=0.405) further underscored the unique clinical value of the CEUS perfusion parameters.

CEUS has been used in the diagnosis of various vascular pathologies (11,14-17), including PAD (16,17,22). Duerschmied et al. (22) compared TICs using CEUS imaging in calf muscles between PAD patients and healthy controls, and found that the PAD patients had a significantly longer TTP (36.9 vs. 19.4 s, P<0.001), indicating decreased muscle perfusion. In another study, Duerschmied et al. (17) localized a boneless area between the proximal and medial third of the gastrocnemius and soleus muscle in an axial plane to acquire the ROIs. The study further revealed that CEUS of the distal calf muscle was a reliable method for determining arterial revascularization. These studies focused on end-organ (calf-muscle) perfusion (16,17,22), with ROIs derived from prespecified tissue and muscle regions.

In our preliminary study, we selected the distal third of the PTA as the ROI for CEUS examination based on its advantages in accessibility, downstream hemodynamic effects, and measurement reliability. First, the PTA is highly accessible due to its consistent superficial course, enabling reproducible examination at any time after EVT, even in cases of severe ischemic reperfusion injury-induced swelling and pain. Second, the PTA is often considered a major downstream outflow during above-knee EVT for PAD (23), with increased blood flow serving as a visual indicator of hemodynamic success. Third, from a technical standpoint, it is easier to localize a specific PTA segment than a boneless muscle area during an examination. This was confirmed in our study, where two radiologists independently evaluated the CEUS perfusion parameters. No significant differences were found between their measurements, and the Bland-Altman analysis showed that the differences were randomly distributed around the mean difference, indicating reliable CEUS perfusion parameters for statistical evaluation.

In this study, the TTP and MTT decreased significantly, and the slope became steeper after EVT, showing that PTA perfusion improved through EVT in PAD. This is consistent with the result of a previous study that showed that popliteal artery perfusion improved after EVT (the TTP decreased from 9.22±3.07 to 5.65±1.02 s) (24). Compared to the TTP, MTT, and slope (i.e., the flow-velocity parameters), the PI, area, AWI, and AWO (i.e., the blood volume parameters) showed no significant increase post-EVT. This might be attributable to microvascular dysfunction in chronic PAD, potentially exacerbated by comorbidities such as DM (present in 39.5% of our cohort), which is known to cause irreversible microvascular impairment. Overall, this study used PTA CEUS perfusion to evaluate EVT-induced hemodynamic changes, thereby addressing a gap in CEUS research at the arterial level. While previous research has shown the clinical utility of CEUS in predicting outcomes such as wound healing in PAD based on muscle perfusion, the predictive value of AWI for wound healing in PAD (odds ratio: 3.4, 95% confidence interval: 1.8–6.3) has also been established (17). Future studies should investigate correlations between these perfusion parameters and clinically meaningful outcomes such as symptom improvement or functional recovery in PAD patients.

This study had several limitations. First, this study only performed CEUS of the PTA, and other downstream vessels, such as popliteal and anterior tibial arteries, were not examined. Second, the study included only 43 patients, a relatively small sample size. Finally, the lack of long-term follow-up might have limited our ability to fully evaluate the sustained effects of EVT on PTA perfusion. Further studies with larger cohorts, different PAD stages, varied treatment strategies, and long-term follow-up need to be conducted to confirm these preliminary results.

Conclusions

The PTA perfusion of PAD patients by CEUS was significantly improved after EVT. These findings show the value of CEUS as a promising adjunct tool for providing detailed hemodynamic insights at the arterial level, with the potential for integration into standard clinical protocols.

Acknowledgments

The authors would like to express our enormous appreciation and gratitude to all participants.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-426/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-426/dss

Funding: This work was supported by the Shanghai Science and Technology Innovation Action Plan (No. 22Y11909500) and Shanghai Science and Technology Industry High Quality Development Plan “Innovative Pharmaceutical and Medical Device Product Application Demonstration” Project (No. 25SF1909005).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-426/coif). W.Z. reports that this work was supported by the Shanghai Science and Technology Innovation Action Plan (No. 22Y11909500) and Shanghai Science and Technology Industry High Quality Development Plan “Innovative Pharmaceutical and Medical Device Product Application Demonstration” Project (No. 25SF1909005). The other 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. This study was approved by the Ethics Committee Institutional Review Board at Huadong Hospital, affiliated to Fudan University (Approval No. 2022K171). Written informed consent was obtained from all patients for the procedures (EVT and CEUS) and for data collection. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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