The use of modern ultrasound tools such as Power Doppler Imaging (PDI) and Microvascular Imaging (MVI) in addition to color-coded Doppler sonography (CCDS) and B-mode in the detection and evaluation of the hepatic artery

Abstract

Objective:

To evaluate the contribution of modern ultrasound imaging tools such as PDI or MVI in improving detection rate, anatomical visualization, and spectral analysis of the hepatic artery.

Methods:

The retrospective single-center study analyzed 40 patients undergoing regular ultrasound control in pre-existing vascular diseases of the liver and after liver transplantation or ablative interventions with furthermore limited examination conditions due to the patient's physique or irregular vascular status after medical treatment such as referred to above. To deal with these conditions, PDI as well as MVI were performed in addition to the standardized B-mode and CCDS. Image quality interpretation was obtained retrospectively by two advanced physicians, evaluating detection rate, anatomical visualization of the vessel itself and artefact-free spectral analysis of the hepatic artery.

Results:

All forty patients (28 men, 13 women, age 23–84 years, mean 60 ± 15 years, median 61 years) showed limited examination conditions and underwent analysis of the resistive index (RI) of the hepatic artery (0.56–0.77, mean 0.67 ± 0.06, median 0.67) by using CCDS, as well as PDI and MVI. The reading addressing the image quality resulted in an average value of 2.74 (median 3.00) ± 0.82 for CCDS in the standard device versus an average value of 3.70 ± 0.83 (median 4.00) in the competing device by combining PDI and MVI scores and when addressed separately 3.56 ± 1.02 (median 4.00) for PDI versus 3.58 ± 1.02 (4.00) for MVI. Overall image quality of the competing device combining PDI and MVI was significantly superior to the standard device only using CCDS for both readers in the detection and evaluation of the hepatic artery (p < 0.01) by providing a strong inter-reader reliability for each evaluation.

Conclusion:

Combination of PDI and MVI can improve detection and visualization of the hepatic artery and its anatomy in compromised examination settings, as well as artefact-free spectral analysis detecting hemodynamic changes.

Keywords

color-coded Doppler sonography power Doppler imaging microvascular imaging hepatic artery imaging quality

Introduction

Color-coded duplex sonography has significantly facilitated the detection of hepatic artery flow compared to standardized Doppler sonography or duplex sonography and, in addition to the classic B-mode image, provides the basis for liver vessel evaluation.¹ Modern high-performance ultrasound machines allow a so-called triplex mode in real-time mode: The visualization of the dynamic B-mode morphology, the color visualization of the flow and the generation of the Doppler spectrum.² This makes it easier to measure the velocity and assess the hemodynamics. The small diameter of sometimes less than 3 mm and frequent variations in anatomical courses mean that advanced examination expertise in sonography is required. A high degree of experience on the part of the investigator is an essential prerequisite for the challenge of clinically valid flow detection in the post-operative setting, for example as part of vascular anastomosis after liver transplantation.^3–7 In order to achieve valid measurements in such critical situations, the examination protocol can be expanded to include additional modalities such as Contrast Enhanced Ultrasound (CEUS),^8,9 Power Doppler Imaging (PDI) and Microvascular Imaging (MVI).^10,11

Through amplitude amplification, Power Doppler Imaging (PDI) is able to provide better images of elongated vessels. It does not use direction coding, but does ultimately remain dependent on the angle of insonation. B-Flow is a digital method of flow detection, comparable to digital subtraction angiography (DSA) and can contribute to the detection of blood flows at both high and low flow velocities simultaneously independent of the angle of insonation. Microvascular Imaging (MVI) uses B-Flow technology, but it amplifies the flow components according to the principle of the PDI with the aim of a visually detectable evaluation of particularly small vessel structures with low flow velocities.

The aim of this study was to evaluate the contribution of modern ultrasound imaging tools such as PDI or MVI in improving detection rate, anatomical visualization, and spectral analysis of the hepatic artery as an expansion to standard examination protocols including only B-mode and CCDS.

Material and methods

This retrospective single-center study analyzed the cases of 40 patients in which in addition to the standard examination protocol, using B-mode and color-coded Doppler sonography (CCDS, Figure 1) for the detection and evaluation of the hepatic artery, Power Doppler Imaging (PDI, Figure 2) and Microvascular Imaging (MVI, Figure 3) were considered necessary due to the patient's physique or irregular vascular status, such as in pre-existing vascular diseases of the liver or after medical treatment such as liver transplantation or ablative interventions, to provide a clear anatomical visualization and artefact-free spectral analysis of the vessel.

Figure 1.

Color-coded Doppler sonography (CCDS) of the liver veins (white arrowheads), portal vein (black asterisk) and the hepatic artery (white arrow) with spectral analysis by using the standard device.

Figure 2.

Power Doppler Imaging (PDI) of the hepatic artery (white arrow) and portal vein (black asterisks).

Figure 3.

Microvascular Imaging (MVI) of the hepatic artery (white arrow), the portal vein (black asterisks)and the cystic artery (white arrowheads) by using the competing device.

Approval for this study was obtained from the Institutional Review Board (IRB) in conformity with the Declaration of Helsinki.¹² The authors comply with the Ethical Guidelines for Publication in Clinical Hemorheology and Microcirculation.¹³

All examinations were performed by a single experienced examiner (more than 3000 examinations per year) on high-end devices (LOGIQ E9 and E10, GE Chicago). The independent reading by a second experienced examiner was performed on the basis of the digitally stored images (PACS). All examinations were performed using a convex ultrasound probe with multi-frequency range with 1–6 MHz (C1–6VN) with the use of depth-adapted flow optimization for color-coded duplex sonography, PDI and MVI. For LOGIQ E10, the image was optimized in terms of depth using automated focus; for LOGIQ E9, the image was individually adjusted to the vessel's region of interest. The B-mode image parameters such as gain, Speckle Reduction Imaging (SRI) or Tissue Harmonic Imaging (THI) were optimized in all cases for the liver hilum. The flow documentation for the liver veins, portal vein and hepatic artery was performed in combination with the B-mode morphology in all cases.

For flow optimization in the color-coded duplex sonography the sample volume (SV) was adjusted to a maximum of two-thirds of the vessel lumen, the pulse repetition frequency (PRF) to peak rates of systolic velocity of 120 cm/s and the color gain to as high as possible, but still without any aliasing at a wall filter setting of 100 Hz. The PDI was adjusted manually (PRF/gain) to obtain the best possible artefact-free flow visualization. With the highest possible speed for the MVI it was possible to select the intensity of the background B-mode image information in three stages (without, with low or with complete overlay) in addition to the manual optimization of the gain in the B-mode image. No change of probes between CCDS, PDI or MVI was necessary, though a low mechanical index (MI) for MVI was obligatory.¹⁴

The independent reading by two radiologists was performed retrospectively using the digitally stored images with regard to a visualization of the course of the vessel of the hepatic artery on the liver hilum that was as artefact-free as possible. All digitally stored images were off-line assessed by independent reading by two investigators with respect to image quality and avoidance of artefacts. A scale was used with 0: not assessable, 1: clear artefacts and poor image quality, 2: artefacts and moderate image quality, 3: satisfactory image quality, proportionate artefacts, 4: good image quality, low artefacts, 5: no artefacts, highest image quality. The criteria for the achievement of the best possible evaluation with regard to the Doppler spectrum were the artefact-free, automatic generation of an envelope curve with evaluation of the peak systolic velocity (PSV) and end diastolic velocity (EDV) as well as the resistive index (RI). No intermediate values were permitted within the framework of this scale. In any cases in which the respective reader had to choose between two scores considered appropriate, therefore, the reader was required to assign the lower value in each case as a means of taking the general problem of inter-individual differences into account as well. A minimum of three consecutive artefact-free Doppler curves were required to derive the flow profile.

The above data, parameters, measurements and evaluations were initially compiled using Microsoft^® Excel and then entered in an SPSS data set for analysis. All data were anonymized and assigned to an individual SPSS-compatible numerical code. The general data analysis, as well as the presentation of the results in graphs, tables and diagrams, was carried out with the assistance of IBM^® SPSS^® Statistics (Version 26.0.0.0), Pages for MacOS, as well as Microsoft^® Word and Microsoft^® Excel.

Statistics

Numerical data were expressed as arithmetic means with standard deviation, and the categorical variables as numbers and percentages. The Wilcoxon rank sum test was used to compare non-normal variables and t-test for normal distribution. The agreement between the two readers in assigning image quality was assessed using Cohen's weighted kappa (κ) statistic. Differences with a p value less than 0.05 were considered significant.

Results

Forty patients (28 men, 13 women) with a mean age 60 ± 15 years from 23 to 84 years (median 61 years) were included. Analyses of the resistive index (RI) of the hepatic artery ranged between 0.56 up to 0.77 (median 0.67) with a mean value of 0.67 ± 0.06. Values between 0.55 and 0.70 are considered as normal.

There were compromised scan conditions in cases of obesity and/or meteorism (17 patients) and anatomical condition variations (23 patients), of which there were 12 patients with condition after ablative liver intervention or transplantation.

The reading addressing the image quality resulted in an average value of 2.74 (median 3,00) ± 0.82 for CCDS in the standard device versus an average value of 3.70 ± 0.83 (median 4.00) in the competing device by combining PDI and MVI scores and 3.56 ± 1.02 (median 4.00) for PDI versus 3.58 ± 1.02 (4.00) for MVI.

The assessments of image quality with inter-rater reliability for the CCDS, PDI and MVI as well as the overall quality of the competing device were assessed by using Cohen's Kappa, a robust measure for qualitative (ordinal) items.

With a kappa of 0.888 ± 0.062, there was strong agreement between the two radiologists when assessing the CCDS in the standard device. The mean rank for image quality was 2.78 for the first reviewer and 2.70 for the second reviewer. The mean ranks did not differ for the two reviewers (p = 0.948). The CCDS image quality scores with inter-rater reliability of reader A versus reader B are shown in Table 1.

Table 1.

CCDS image quality scores for standard device of reader A versus reader B.

		Reader B
	Score	0	1	2	3	4	5	n (%)
Reader A	0	0	0	0	0	0	0	0
	1	0	2	0	0	0	0	2 (5.0)
	2	0	1	12	0	0	0	13 (32.5)
	3	0	0	0	17	0	0	17 (42.5)
	4	0	0	0	2	6	0	8 (20.0)
	5	0	0	0	0	0	0	0
	n (%)	0	3 (7.5)	12 (30.0)	19 (47.5)	6 (15.0)	0	40
Weighted Kappa^a (κ)			0.888
Standard error (SE)			0.062
95% Confidence Interval (CI)			0.767–1.000

Linear weight.

With a kappa of 0.925 ± 0.052, there was strong agreement between the two radiologists when assessing the overall image quality of the competing device combining PDI and MVI. The mean rank for image quality was 3.70 for both reviewers. The PDI image quality scores with inter-rater reliability of reader A versus reader B are shown in Table 2.

Table 2.

Overall image quality scores for competing device of reader A versus reader B.

		Reader B
	Score	0	1	2	3	4	5	n (%)
Reader A	0	0	0	0	0	0	0	0
	1	0	0	0	0	0	0	0
	2	0	0	1	1	0	0	2 (5.0)
	3	0	0	0	16	0	0	16 (40.0)
	4	0	0	0	1	13	0	14 (35.0)
	5	0	0	0	0	0	8	8 (20.0)
	n (%)	0	0	1 (2.5)	18 (45.0)	13 (32.5)	8 (20.0)	40
Weighted Kappa^a (κ)			0.925
Standard error (SE)			0.052
95% Confidence Interval (CI)			0.824–1.000

Linear weight.

Judged overall image quality of the competing device combining PDI and MVI was significantly superior to the standard device only using CCDS for both readers (reader A: p < 0.0001; reader B: p < 0.0001) in the detection and evaluation of the hepatic artery (p < 0.01). In 32 cases the competing device was ranked at least one grade higher, in 8 cases with equal results and in none of the cases inferior to the standard device.

PDI and MVI in combination necessary due to inter-individual differences, with otherwise equal quality values in 30 cases. When considered separately, by comparison, the MVI was favored versus the PDI in 6 patients and the PDI favored versus the MVI in 4 patients.

With a kappa of 0.898 ± 0.056, there was strong agreement between the two radiologists when assessing the PDI. The mean rank for image quality was 3.55 for the first reviewer and 3.58 for the second reviewer. The PDI image quality scores with inter-rater reliability of reader A versus reader B are shown in Table 3.

Table 3.

PDI image quality scores of reader A versus reader B (competing device).

		Reader B
	Score	0	1	2	3	4	5	n (%)
Reader A	0	0	0	0	0	0	0	0
	1	0	1	0	0	0	0	1 (2.5)
	2	0	0	4	2	0	0	6 (15.0)
	3	0	0	0	11	0	0	11 (27.5)
	4	0	0	0	1	13	0	14 (35.0)
	5	0	0	0	0	0	8	8 (20.0)
	n (%)	0	1 (2.5)	4 (10.0)	14 (35.0)	13 (32.5)	8 (20.0)	40
Weighted Kappa^a (κ)			0.898
Standard error (SE)			0.056
95% Confidence Interval (CI)			0.787–1.000

Linear weight.

With a kappa of 0.931 ± 0.047, there was strong agreement between the two radiologists when assessing the MVI. The mean rank for image quality was 3.58 for both reviewers. The MVI image quality scores with inter-rater reliability of reader A versus reader B are shown in Table 4.

Table 4.

MVI image quality scores of reader A versus reader B (competing device).

		Reader B
	Score	0	1	2	3	4	5	n (%)
Reader A	0	0	0	0	0	0	0	0
	1	0	1	0	0	0	0	1 (2.5)
	2	0	1	3	0	0	0	4 (10.0)
	3	0	0	0	13	1	0	14 (35.0)
	4	0	0	0	0	13	0	13 (32.5)
	5	0	0	0	0	0	8	8 (20.0)
	n (%)	0	2 (5.0)	3 (7.5)	13 (32.5)	14 (35.0)	8 (20.0)	40
Weighted Kappa^a (κ)			0.931
Standard error (SE)			0.047
95% Confidence Interval (CI)			0.893–1.000

Linear weight.

Discussion

Visualizing the morphology and measuring the hemodynamics is essential for comprehensive liver ultrasound diagnostics. For example, liver cirrhosis with portal hypertension or cavernous transformation of the portal vein in the case of thrombosis leads to a progressive increase in flow and dilatation of the hepatic artery. The same also applies in cases of hereditary hemorrhagic telangiectasia (HHT) involving the formation of intrahepatic shunt systems. In these cases of hemodynamic changes in particular, the assessment of hemodynamics with color-coded duplex sonography is often easier than in normal cases. These situations in particular would even allow for the use of handheld ultrasound devices (HUDs), given the circumstances of an uprising availability over the years¹⁵ with a boost during the recent SARS-CoV-2 pandemic¹⁶ and its feasibility in bedside-usage¹⁷ paired with reliable image quality especially in visualizing the hepatic artery.¹⁸

However, complications arise with reduced flow rates or a narrowing of the vessel lumen. In this case, morphological aspects also play a role in addition to purely hemodynamic aspects: Dissections or stenosis of the hepatic artery after liver transplantation in the intrahilar course, as well as thrombosed pseudoaneurysms or wall-adherent arterial thrombi. In these cases, flow detection using color-coded duplex sonography – as the most widely available and most highly validated vascular ultrasound modality – is often considerably more difficult than is normally the case. In the event of hepatic artery occlusion (HAO), further differentiation of the underlying causes mentioned above can be addressed by using Contrast Enhanced Ultrasound (CEUS).¹⁹ Especially when contrast enhanced angiographic examination by computed tomography (CT) or magnetic resonance imaging (MRI) are not feasible: critically ill patients with severe kidney failure, high risk during transportation outside the intensive care unit or restrictions due to the magnetic field itself (e.g., non-MRI-conditional pacemakers). There are also underlying physical and technical aspects that contribute to the disadvantages of color-coded duplex sonography. These include the considerable angle dependence of the imaging, which means that the hands of an experienced examiner are required in order to achieve a high degree of diagnostic accuracy. Numerous flow artefacts must also be taken into account, aliasing in particular.

Although Power Doppler Imaging (PDI) can close this gap in the detection of smaller and partially elongated vessels with higher sensitivity to a certain extent, this method also remains dependent on the angle and on the experience of the examiner. Alternative digital flow methods such as MVI were used to attempt flow visualization of both high and low flow rates with no aliasing which, in addition to the visualization of the macrovascularization, also allows the diagnosis of the microvascularization.²⁰ In addition to the general constraints of sonography, the limitations of MVI are evident in its clear depth dependence and susceptibility to artefacts due to motion,¹⁴ moreover not every ultrasound device even provides the tool. The B-Flow additionally provides an angle-independent tool with an almost equally high sensitivity regarding low flow vascularization.²¹

With respect to the challenges referred to above, a combination of PDI and MVI as an addition to color-coded Doppler sonography proved to be the diagnostic method of choice in the present study, which was conducted for the first time in this way. This does not mean that the evaluation used to date by means of B-mode image and in particular color-coded duplex sonography is no longer necessary. Rather, it is considered as a useful additional step to enable vessels altered by surgery or underlying vascular diseases as well as physiological anatomic variation to be identified more easily, to visualize them more effectively and thus enable the sample volume to be placed more precisely.

The addition of the MVI to existing standard examination protocols would appear to offer benefits in other respects as well. Being non-invasive, since as a method it does not involve a contrast medium – unlike angiography with computed tomography – and is also less complex to perform, MVI is also a good alternative compared to Contrast Enhanced Ultrasound (CEUS) for the differentiation of benign from malignant superficial lymph nodes.²² In this connection, other new methods of visualization of the vessel should also be considered. Though already delivering reliable flow visualization and quantification in even complex pulsatile structures,²³ model-based studies and clinical applications for Vector Flow Imaging (VFI) at this point first and foremost include diseases of the heart and large vessels, rather than the evaluation of smaller vessels such as the hepatic artery, not to mention microvascularization.^24–26 Although subject to the same limitations of depth dependence as the MVI, methods such as Ultra Micro Angiography (UMA) already make diagnostic contributions to the evaluation of superficial processes such as, for example, lipedema²⁷ or rheumatoid arthritis.²⁸ With regard to the optimization of macrovascular processes, the application of High-Resolution Flow (HR Flow) and Glazing Flow is becoming increasingly established. In combination, both methods effectively complement color-coded duplex sonography by providing valid detection of morphological and hemodynamic changes in both hepatic arteries and portal veins within the liver.²⁹ The diagnostic added value of combined examination protocols and the knowledge of alternative measurement methods is therefore crucial to meet the respective challenges of the examination effectively.

Physical limitations of ultrasound cannot be overcome, but the results indicate the diagnostic potential of new digital measurement methods for the hepatic artery for increasingly precise questions. Only newer generation devices offer these modalities, however, and the underlying technical and mathematical principles vary from company to company. A device-independent comparison should therefore be undertaken in multi-center studies.

Footnotes

ORCID iD

M Akers

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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