Preliminary exploration of quantitative analysis parameters of renal cortical blood perfusion by contrast-enhanced ultrasound in hypertensive patients

Introduction

Hypertension is a major global public health issue and a leading risk factor for end-organ damage, particularly hypertensive nephropathy, which significantly increases the risk of chronic kidney disease progression (1,2). Chronic elevated blood pressure induces structural remodeling and functional rarefaction of the renal microvasculature, directly leading to decreased renal cortical blood perfusion (RCBP) and diminished renal blood flow reserve (3,4). Capturing these early alterations in renal blood perfusion may greatly facilitate personalized and precise diagnostic and therapeutic strategies for patients with hypertension.

Contrast-enhanced ultrasound (CEUS) is a novel imaging technique that enhances blood flow signals and clearly displays renal microcirculation perfusion by intravenously injecting ultrasound contrast agents. Compared to traditional ultrasound, quantitative analysis with CEUS allows for a more accurate quantitative assessment of RCBP (5-7). Previous experimental and clinical studies have validated the capacity of CEUS-derived parameters to quantify renal cortical microvascular perfusion (5,8,9). However, existing literature has predominantly focused on cohorts with established renal impairment, such as patients with advanced chronic kidney disease or diabetic nephropathy (10,11). For instance, in patients with chronic kidney disease, Han and Park found that specific perfusion-related parameters, such as the wash-in rate and wash-out rate, are significantly decreased compared to healthy controls (12). Similarly, Ma et al. reported that patients with advancing diabetic kidney damage exhibit a markedly prolonged time to peak (TTP) alongside a significant decrease in peak intensity (PI) (10). Despite the proven utility of CEUS in advanced disease stages, there remains a conspicuous paucity of research evaluating renal cortical perfusion in healthy populations or in patients with preserved renal function, such as hypertensive patients without renal impairment.

We retrospectively analyzed the RCBP data of 83 hypertensive patients, none of whom had renal artery stenosis (RAS), renal function abnormalities, or anti-hypertension therapy. Due to suspected hypertension, these patients underwent renal CEUS examination (including renal artery and RCBP). These patients were not a completely normal population, but they did not have diabetes, RAS, or abnormal renal function. In actual clinical practice, patients requiring renal CEUS examination are mostly due to hypertension investigation. Summarizing the RCBP parameters of these patients still has positive significance. Thus, we made a descriptive characterization of RCBP parameters in this specific population, with reproducibility assessment conducted. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2751/rc).

Methods

Patients

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Beijing Hospital (No. 2019BJYYEC-017-01), and the requirement for individual consent for this retrospective analysis was waived. We recruited 83 hypertensive patients who underwent RCBP CEUS at the Department of Ultrasound Medicine, Beijing Hospital, between October 2020 and June 2023. All of them were confirmed to be free of RAS by a comprehensive ultrasound protocol (including grayscale imaging, color Doppler, spectral Doppler, and renal artery CEUS to evaluate luminal morphology and hemodynamics, and contrast agent beam width), and only a subset of patients had additional confirmation by computed tomographic angiography (CTA) or magnetic resonance angiography (MRA). The cases included 45 males and 38 females, aged 34–86 years and with an average age of 61.59±14.42 years. The elderly were defined as individuals aged 60 years or older, which is consistent with the statutory retirement age in China and used in some Chinese clinical guidelines and epidemiological studies (13,14). The inclusion criteria were as follows: age ≥18 years; hypertension without antihypertensive medication; absence of RAS and diabetes; and normal renal function [estimated glomerular filtration rate (eGFR) ≥90 mL/min/1.73 m²]. The exclusion criteria were as follows: poor quality ultrasound images; allergy to ultrasound contrast agents; and renal anatomical abnormalities including renal cysts, tumors, hydronephrosis, or other structural renal disorders.

Data collection

The contrast agent used was Sonovue (Bracco, Milan, Italy). The instrument used for CEUS examination: Samsung RS80A Ultrasound Diagnostic Instrument (Samsung, Seoul, Korea) with a CA1-7 convex array probe, operated at a frequency range of 2–5 MHz and machine parameters set to a mechanical index of 0.079 and gain of 56 dB. Patients were required to fast for 8–12 hours, and took the lateral position. After the long axis of the kidney was clearly displayed and perpendicular to the ultrasound beam, the contrast mode was initiated while the patient breathes calmly, and a bolus of 1.2 mL SonoVue was injected via a 3-way stopcock in the antecubital vein and flushed with 5 mL 0.9% saline immediately. The probe was held freehand by the operator to maintain the kidney in the maximum longitudinal plane, with its orientation kept perpendicular to the renal long axis. The perfusion cine loop was continuously acquired and dynamically observed for 3 minutes. The above procedure is repeated for the contralateral kidney after an interval of at least 15 minutes to ensure complete clearance of SonoVue (7), with visual confirmation made that the contrast-mode image returned to pre-injection appearance. The scanning order of the left and right kidneys was randomized to minimize systematic bias. RCBP analysis was performed using the built-in analysis software of the Samsung RS80A ultrasound diagnostic system. A circular region of interest (ROI) with a diameter of approximately 5 mm was selected in the middle part of the kidney to generate the time-intensity curve (TIC). The built-in analysis software provided real-time ROI tracking to compensate for minor motion artifacts during the acquisition. An automated intensity threshold algorithm was used to define time-zero (start of the wash-in phase). TIC analysis was performed using the system’s default wash-in/out model (Gamma-Variate Model), which was selected as it is the manufacturer’s officially recommended algorithm for extracting RCBP parameters on this ultrasound platform. Using Gamma-Variate Model, RCBP parameters were extracted, including PI, rise time (RT), mean transit time (MTT), area under the curve (AUC), wash-in area under the curve (iAUC), wash-out area under the curve (oAUC), and TTP, PI/MTT, totaling 8 parameters. TIC quantitative analysis is performed on linearized intensity data, with dB used only for display. Three such ROIs were selected, and the average values of each parameter were taken as the final measured values for analysis (Figure 1). Through stratified analysis, the characteristics of RCBP parameters were analyzed for left/right side, different sexes, and elderly versus non-elderly individuals.

Figure 1 Contrast-enhanced ultrasound analytical image of renal cortex blood flow perfusion. A circular ROI with a diameter of approximately 5 mm was selected in the middle of the kidney to generate a TIC. The intensity axis is presented in a log-compressed dB scale for better visualization. The red, green, and yellow circles in the image represent the three selected ROIs. The red, green, and yellow curves at the bottom left of the image correspond to the three TICs generated from the respective ROIs. The table at the bottom right of the image displays the renal cortical perfusion parameters, including PI, RT, MTT, AUC, iAUC, oAUC, and TTP. AUC, area under the curve; iAUC, wash-in area under the curve; MTT, mean transit time; oAUC, wash-out area under the curve; PI, peak intensity; ROI, region of interest; RT, rise time; TIC, time-intensity curve; TTP, time to peak.

Inter-observer agreement assessment

Two designated senior sonographers with over 10 years of clinical experience in renal CEUS independently performed ROI placement and quantitative extraction of RCBP parameters on the same stored renal CEUS cine loops in a blinded manner, with inter-observer consistency of all parameters subsequently evaluated.

Statistical analyses

SPSS 25.0 statistical software (IBM Corp., Armonk, NY, USA) was used. Counting data were presented as either the percentage of cases, whereas measurement data were reported as mean ± standard deviation if they followed a normal distribution, or as median and interquartile range (IQR; 25th–75th percentile) if they did not. Differences between groups for normally distributed continuous variables were compared using t-tests or analysis of variance (ANOVA), whereas Mann-Whitney U tests or Kruskal-Wallis H tests were used for non-normally distributed data. For paired comparisons between the left and right kidneys (within the same patient), paired t-tests were used for normally distributed parameters, and the Wilcoxon signed-rank test was adopted for non-normally distributed parameters. Inter-observer agreement assessment was assessed using the intraclass correlation coefficient and Bland-Altman method. A P value <0.05 was considered statistically significant.

Results

Clinical characteristics of 83 patients

Among the 83 patients, 45 were male and 38 were female. There were sex differences in height and weight (P<0.001), but no statistically significant sex differences were found in age, heart rate, systolic blood pressure, or diastolic blood pressure (P>0.05) (Table 1).

Comparison of RCBP parameters between the right and left kidneys

The 83 patients (166 kidneys in total) were stratified into left and right kidney groups sides for comparative analysis of RCBP parameters. It showed that the PI and MTT of the right side were smaller than those of the left side, whereas RT, AUC, iAUC, oAUC, TTP, and PI/MTT were larger than those of the left side, but none of these differences were statistically significant (P>0.05) (Table 2 and Figure 2).

Figure 2 Comparison of renal cortical blood perfusion parameters across different subgroups. Box plots show the median, interquartile range, and min/max values (whiskers) for each RCBP parameter. Three pairwise subgroup comparisons are presented: left vs. right, male vs. female, and elderly vs. non-elderly. *, P<0.05; **, P<0.01. (A) PI; (B) RT; (C) MTT; (D) AUC; (E) iAUC; (F) oAUC; (G) TTP; (H) PI/MTT. AUC, area under the curve; iAUC, wash-in area under the curve; MTT, mean transit time; oAUC, wash-out area under the curve; PI, peak intensity; PI/MTT, ratio of peak intensity to mean transit time; RCBP, renal cortical blood perfusion; RT, rise time; TTP, time to peak.

Comparison of renal cortical perfusion parameters between different sex groups

Dividing the 83 patients into male group and female group, the results showed that the iAUC and TTP in males were greater than in females, with the differences being statistically significant (P<0.05). The PI, RT, MTT, and PI/MTT in males were greater than in females, whereas the AUC and oAUC were smaller than in females, but all these differences were not statistically significant (P>0.05) (Table 3 and Figure 2).

Comparison of renal cortical perfusion parameters between elderly and non-elderly groups

Eight-three patients were divided into two groups based on age: non-elderly group (18-59 years old) and elderly group (≥60 years old). The MTT and TTP in the elderly group were greater than those in the non-elderly group, showing an increasing trend with age, and the differences were statistically significant (both P<0.05). Conversely, PI/MTT in the elderly group was smaller than that in the non-elderly group (P<0.01). The RT and iAUC in the elderly group were greater than those in the non-elderly group, whereas the PI, AUC, and oAUC were smaller than those in the non-elderly group, but the differences were not statistically significant (P>0.05) (Table 4 and Figure 2).

Inter-observer agreement analysis

For the inter-observer agreement analysis of RCBP parameters, 32 patients (64 kidneys) were randomly selected from 83 patients. The intraclass correlation coefficient (ICC) for inter-rater reliability of PI, RT, MTT, AUC, iAUC, oAUC, and TTP are detailed in Table 5. The Bland-Altman plot demonstrated good inter-rater agreement for RCBP (Figure 3). Notably, time-related parameters exhibited higher inter-observer reproducibility than intensity-based parameters. For instance, TTP yielded a higher ICC value of 0.873, whereas RT showed a relatively lower ICC of 0.668.

Figure 3 Bland-Altman plot for renal cortical blood perfusion parameters. (A-G) Inter-rater agreement analysis for renal cortical blood perfusion parameters: (A) PI; (B) RT; (C) MTT; (D) AUC; (E) iAUC; (F) oAUC; (G) TTP. AUC, area under the curve; iAUC, wash-in area under the curve; MTT, mean transit time; oAUC, wash-out area under the curve; PI, peak intensity; ROI, region of interest; RT, rise time; SD, standard deviation; TIC, time-intensity curve; TTP, time to peak.

Discussion

Currently, there is relatively limited research on the characteristics of RCBP parameters in hypertensive patients, and the parameters analyzed and compared in various studies differ, including PI, MTT, AUC, and TTP. Our study encompasses a broader and more diverse set of RCBP parameters, including PI, RT, MTT, AUC, iAUC, oAUC, and TTP. Notably, in this study, we introduced the composite index PI/MTT, which integrates both signal intensity and temporal parameters, thereby potentially providing a more accurate and comprehensive reflection of true microvascular perfusion function (15,16). Previous research indicated that, at rest, female hypertensive patients exhibit higher cortical micro perfusion than males (17), which was derived from the measurement of the cortical perfusion index using the dedicated software Vuebox (Bracco Research, Geneva, Switzerland). The authors explained that the reason for this result might be the protective effect of estrogen in women on endothelial cells. The average age of the women in the above study was 46.5±15.0 years, which corresponded to the age stage with higher estrogen levels. In our study population, the average age of women was 61.84±13.40 years, with the majority being in a postmenopausal state with lower estrogen levels. The average age of men in our study was 61.38±15.37 years, and there was no statistically significant difference in age between men and women (P=0.981). Under the premise of age matching, the final analysis showed no statistically significant difference in renal blood perfusion between men and women (P>0.05), which aligns with previous literature suggesting that the cardiovascular risk characteristics of postmenopausal women were similar to those of age-matched men (18,19).

We retrospectively analyzed the RCBP parameters in a group of adult hypertensive patients without RAS, aiming at providing references and evidence for early assessment of renal cortical perfusion. The study of CEUS parameters has practical clinical significance and scientific research exploration value. Conventional ultrasound mainly relies on changes in renal structure, including kidney size, morphology, and changes in renal echo for the assessment of renal function, being incapable of assessing blood flow perfusion. In the early stages of diabetic nephropathy and membranous nephropathy, there are no obvious morphological changes, whereas cortical perfusion has significantly decreased (10,20). Also, the quantitative dynamic CEUS can effectively evaluate renal parenchymal perfusion and identify hemodynamic abnormalities associated with urinary tract obstruction (21). At this point, CEUS can quantify the hemodynamic characteristics of renal microcirculation, reflect hemodynamic changes associated with glomerular filtration and renal vascular resistance, and can detect perfusion abnormalities before structural changes, providing evidence for early clinical intervention (22,23). In addition to enabling early diagnosis, CEUS is also valuable in dynamic monitoring of kidney disease progression and treatment efficacy, such as assessing the progression of chronic kidney disease, evaluating the impact of drugs on renal blood perfusion, assessing the blood perfusion of transplanted kidneys, and evaluating changes in renal cortical perfusion parameters after interventional surgery to determine the effectiveness of vascular recanalization (24-29). Some studies have shown that CEUS can detect acute renal hemodynamic changes induced by drugs (9,30).

When it comes to the widespread clinical application of quantitative analysis in CEUS, challenge lies in the reproducibility among different observers, as poor consistency may lead to unreliable results. To minimize inter-observer heterogeneity, we conducted pre-job training for physicians, unifying standards in the process of image and data processing, such as the size of the ROI, and its placement location. The final analysis results demonstrate that the correlation coefficients in the reproducibility tests of all quantitative parameters range between 0.668 and 0.873, demonstrating good consistency among different observers and the reliability of the measurement method, which aligns with the results of previously published research (31). This was interpreted with reference to the criteria by Cicchetti (32), where an ICC of >0.75 is considered excellent, 0.60–0.74 is good, 0.4–0.59 is fair, and <0.40 is poor. Furthermore, time-related parameters presented higher reproducibility compared with intensity-based parameters. This consistent trend is in line with the findings from Averkiou et al., which confirmed that CEUS time-related parameters generally possessed better reproducibility than intensity-based parameters across different ultrasound platforms and analytical software packages (33).

It is also important to recognize the following limitations. Firstly, although the patients included in this study were all screened to exclude RAS and renal dysfunction, they were all hypertensive patients and not truly healthy individuals. The diagnosis and exclusion of RAS were mainly based on conventional ultrasound and renal artery CEUS, rather than the gold reference standard digital subtraction angiography (DSA). Although consistent with routine clinical practice, this constitutes a potential limitation of the study. It has been suggested that hypertensive patients have lower cortical perfusion compared to normotensive participants (3), and that the cases should be carefully considered when applying our research findings. In addition, cardiovascular comorbidities were not systematically documented in this study, which may also confound the present results, as such conditions have been reported to independently affect renal cortical perfusion parameters (34,35). Secondly, multiple comparison correction was not applied in the subgroup analyses of renal cortical perfusion parameters, primarily owing to the limited overall sample size. Strict correction under this condition would markedly increase the risk of Type II errors and mask potential exploratory trends in perfusion parameters. Furthermore, after correction for multiple comparisons, none of the reported differences reach statistical significance. Also, we did not explore the interactive effects of laterality, gender, and age on renal perfusion parameters, because limited sample size lacked sufficient statistical power for such interaction analysis. Thus, subgroup findings are interpreted as suggestive rather than definitive, and caution is advised in their clinical interpretation. Future studies with larger sample sizes should refine stratification and apply appropriate statistical corrections to validate these observations. Moreover, a fixed contrast agent dose (1.2 mL) was used without weight adjustment, which may introduce intersubject variability in perfusion parameters and represents a potential limitation of this study (7). Lastly, all RCBP parameters in this article were obtained using on-machine analysis software of the Samsung RS80A ultrasound diagnostic system, and may not be comparable with other parameters derived from different devices and analysis software.

Conclusions

In summary, this study preliminarily explored the characteristics of RCBP parameters in adult hypertensive patients without RAS and renal insufficiency, and further validated the good reproducibility of quantitative analysis techniques using CEUS. It should be noted that reference values are subject to individual variations due to factors such as age, body size, examination equipment, and analysis methods. In practical work, RCBP parameters should be applied in conjunction with other examinations to get a comprehensive assessment.

Acknowledgments

We are grateful to the radiologists and technicians for their valuable contributions to this study.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2751/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2751/dss

Funding: This work was supported by the National High Level Hospital Clinical Research Funding (Nos. BJ-2018-198 and BJ-2023-096) and Beijing Science and Technology Project (No. Z211100002921011).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2751/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 Ethics Committee of Beijing Hospital (No. 2019BJYYEC-017-01), 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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