When performing conventional brightness-mode ultrasonography in dogs and cats, identifying diffuse hepatic disease is more challenging than identifying focal hepatic disease because of the lower degree of alteration in the hepatic parenchymal echotexture with diffuse disease.1 Moreover, the ultrasonographic appearances of diffuse hepatic diseases overlap considerably, rendering differentiation among them difficult.2,3 The ultrasonographic features of the liver, including its echogenicity, echotexture, portal venous clarity, borders, and edges, are insufficient to enable the accurate identification of diffuse hepatic diseases.2 Although histopathologic examination is the gold standard for accurate diagnosis and monitoring of diffuse hepatic disease, hepatic biopsy may be contraindicated because of the risk of bleeding complications and the need to administer general anesthesia to critically ill patients. Therefore, it is necessary to develop noninvasive methods to evaluate hepatic diseases quantitatively in veterinary medicine.4,5
Vacuolar hepatopathy in dogs and hepatic lipidosis in cats constitute the most common diffuse hepatic diseases that result in increased hepatic echogenicity.6 Vacuolar hepatopathy is a disease characterized by the development of vacuoles in the hepatocytes that are filled with fat, glycogen, or water. Steroid-induced hepatopathy and hepatic steatosis are types of vacuolar hepatopathy.7,8 Previous studies9–11 that induced vacuolar changes experimentally in the hepatocytes of dogs and cats reported increased attenuation of the liver, and revealed that quantitative measurement of attenuation could be used to evaluate accurately the acoustic change in the liver with subclinical lipid infiltration.
The term attenuation refers to the phenomenon in which the amplitude and intensity of ultrasonic waves decrease as the waves penetrate the tissue.12 The attenuation coefficient (AC) denotes the degree of attenuation and is expressed in decibels per centimeter per megahertz.13 Attenuation is mainly influenced by 3 mechanisms: absorption, scattering, and reflection.14 Absorption is the conversion of sound energy into heat when the ultrasound beam is transferred to the propagating medium.15 Scattering is the phenomenon that occurs when sound waves strike tissues that are much smaller relative to the ultrasound wavelength.15,16 The degree of scattering is relatively less than the intensity of the reflected echo in soft tissues, and its contribution to overall attenuation is relatively small.16,17 Reflection occurs when the sound beam encounters materials with large boundaries that are smooth and continuous, and that are larger relative to the ultrasound wavelength.15,16,18 If an ultrasound beam encounters acoustic boundaries, some energy is reflected while the residual beam energy is transmitted through the interface.15,16
Attenuation imaging (ATI) is an ultrasound-based application that estimates the AC of soft tissues, and is currently available with a commercial ultrasonography system (Aplio i-series, Canon Medical Systems). The ATI system automatically removes the influence of gain control and focus-dependent beam profiles from the image and yields the adjusted intensity, providing the AC. If the area to be measured is set, the system receives the adjusted returning echo signal and calculates the AC according to the formula
Most studies12,13,19–24 of ATI in humans have been based on a consistent examination method that entails scanning the right lobe of the liver at the intercostal space. Some studies acquired the ACs while asking participants to hold their breath12,19,20,24–26 and placed the ROI box at least 2 cm below the liver capsule.20,22,24 However, no study presented a clear rationale for these protocols or evaluated technical factors influencing the ACs.
Thus, the objectives of the study reported here were to investigate the clinical feasibility of the hepatic parenchyma in healthy Beagles, identify technical factors that influenced measured ACs, and determine intraobserver repeatability of measurements.
Materials and Methods
Animals
Ten male Beagles (9 sexually intact and 1 castrated) were included in the study. Mean age was 2 years (range, 1 to 9 years), and mean body weight was 9.8 kg (range, 7.9 to 11.0 kg). All dogs were determined to be healthy on the basis of results of a physical examination, CBC, serum biochemical panel, radiography, abdominal ultrasonography, and echocardiography. The study protocol was approved by the Institutional Animal Care and Use Committee of Konkuk University (approval No. KU21176).
Acquisition protocol for ATI
All ATI examinations were performed with a commercial ultrasonography machine (Aplio i800 ultrasound machine, Canon Medical Systems) with a 1.8- to 6.4-MHz convex probe (PVI-475BX). All dogs were fasted for at least 12 hours before the examination, and hair over the entire cranial aspect of the abdomen and last 3 intercostal spaces was clipped. Dogs were examined without sedation or anesthesia. They were positioned in dorsal recumbency, and coupling gel was applied to minimize the occurrence of ultrasound artifacts. During the ATI examination, the real-time grayscale mode was visible on the left side, and the attenuation color map mode was shown on the right side of the monitor (Figure 1). The entire scan depth was set to 8 cm in all dogs. Because the accessible area of the dogs’ liver is smaller than that of humans, both the trapezoidal-shaped attenuation color map and ROI box were set to 20 mm (width) X 30 mm (length), the smallest size allowed by the system. Although large vessels and echogenic materials were excluded automatically in the color map, the ROI box was positioned to avoid the bile duct and vessels to reduce artifacts and acquire a more reliable measurement. After the ROI box was placed in the appropriate position and the image was frozen, the AC and coefficient of determination (R2) were observed at the bottom of the display. Data quality was classified as excellent (R2 ≥ 0.9), good (0.9 > R2 ≥ 0.8), or poor (R2 < 0.8), and only data with an R2 value ≥ 0.8 were used, whereas all data with an R2 value < 0.8 were discarded, as recommended.19,20,23–25 Examinations were repeated 5 times for each measurement technique, and mean AC values were used for statistical analyses.
Sample image obtained during ultrasonographic attenuation imaging of the hepatic parenchyma in a dog at a scanning depth of 10 to 20 mm. The real-time grayscale image is shown on the left side, and the attenuation color map mode is shown on the right side. The size of the region of interest box is 20 mm (width) X 30 mm (length). The scan depth is the distance between the hepatic capsule and the top of the region of interest box (double-headed arrow). The values of the attenuation coefficient and coefficient of determination are shown at the bottom of the screen.
Citation: American Journal of Veterinary Research 83, 8; 10.2460/ajvr.21.11.0194
Technical factors influencing the ACs
The ACs were acquired 16 times for each dog by altering the 5 following conditions: scanning plane, measurement site, scanning depth, scanning approach, and breathing conditions. For scanning plane, measurements were acquired in the transverse and sagittal planes. For measurement site, the left and central divisions of the liver were examined (Figure 2). Considering the anatomic location of the liver, the lateral parts of the left lateral and left medial lobes were designated as the left division of the liver. The papillary process of the caudate lobe, quadrate lobe, medial part of the left lateral lobe, and left medial lobe were designated as the central division of the liver. The right medial lobe, right lateral lobe, and caudate process of the caudate lobe were excluded because it was difficult to approach these areas as a result of interference by the gallbladder. For scanning depth, the upper region of the liver in the near field was excluded, and 2 scanning depths (10 to 20 mm and 20 to 30 mm) were selected to prevent reverberation artifacts of the skin and liver capsule. The scanning depths were determined on the basis of the distance between the liver capsule and the top of the ROI box (Figure 1). With regard to scanning approach, examinations were conducted via the intercostal and subcostal approaches. The transducer was placed perpendicular to the dog’s skin for the intercostal transverse method and parallel to the ribs while conducting measurements in the transverse plane to avoid acoustic shadowing artifacts of the ribs as much as possible. The left division of the liver was examined with the left intercostal approach, and the central division of the liver was examined with the right intercostal approach. For the subcostal approach, the angle between the transducer and the dog’s abdomen was 30° to 45° for optimal visualization of the liver. With regard to breathing conditions, the left division of the liver was examined through the left intercostal transverse approach at a depth of 10 to 20 mm, and the central division of the liver was examined through the subcostal transverse approach at a depth of 10 to 20 mm while gently covering the nose of the dog with a hand for 2 seconds at an end-expiration period to compare values obtained when dogs were breathing freely versus breath-holding at end expiration.
Schematic diagrams of the canine liver in the ventrodorsal view (A) and in cross-section at the level of the porta hepatis (B). The liver is divided into the right (I), central (II), and left (III) divisions. The right medial lobe (L5), right lateral lobe (L6), and caudate process of the caudate lobe (not depicted in the figure) are designated as the right division (I) of the liver. The papillary process of the caudate lobe (L1), quadrate lobe (L4), medial part of the left lateral lobe (L2), and left medial lobe (L3) are designated as the central division (II) of the liver. The lateral parts of L2 and L3 are designated as the left division (III) of the liver.
Citation: American Journal of Veterinary Research 83, 8; 10.2460/ajvr.21.11.0194
Examinations were repeated during 3 sessions for each dog. Sessions 1 and 2 were performed on the same day, with an interval of at least 20 minutes. Session 3 was performed at least 6 days after session 2. All examinations were conducted by the same investigator (YEL) with expertise in diagnostic imaging.
Statistical analysis
The ACs were summarized as mean ± SD. The distribution of AC values was analyzed with the Kolmogorov-Smirnov test. Independent t tests were used for normally distributed data, and the Mann-Whitney test was used for non-normally distributed data to evaluate differences in measurement sites, scanning planes, breathing conditions, scanning depths, and scanning approaches. Intraobserver repeatability was assessed by comparing AC values between sessions 1 and 2 (intraday reliability), and sessions 1 and 3 (interday reliability) with intraclass correlation coefficients (ICCs). In addition, ICCs for scanning plane, measurement site, scanning depth, and scanning approach in sessions 1 and 2 were computed to evaluate repeatability. On the basis of the 95% CI, reliability was classified as poor (ICC < 0.5), moderate (0.5 < ICC < 0.75), good (0.75 < ICC < 0.9), or excellent (ICC ≥ 0.9).27 All statistical analyses were conducted with standard software (SPSS, version 25; IBM Corp). Values of P < .05 were considered significant.
Results
Technical factors influencing the ACs
No significant differences (P = .120 to 1.000) were observed in the ACs between the transverse and sagittal scanning planes (Table 1) or between the left and central divisions of the liver (P = .292 to .848). The ACs measured at 20 to 30 mm from the liver capsule were significantly (P < .01) less than those measured at 10 to 20 mm (Figure 3). The ACs obtained via the subcostal approach were significantly (P < .05) greater than those obtained via the left and right intercostal approaches (Figure 4).
Mean ± SD attenuation coefficient of the hepatic parenchyma in 10 healthy Beagles.
| Scanning plane (dB/cm/MHz) | |||||
|---|---|---|---|---|---|
| Measurement site | Scanning approach | Scanning depth (mm) | Transverse | Sagittal | P value |
| Left division | |||||
| Left intercostal | |||||
| 10–20 | 0.65 ± 0.050 | 0.65 ± 0.067 | 1.000 | ||
| 20–30 | 0.54 ± 0.052 | 0.52 ± 0.054 | .435 | ||
| Subcostal | |||||
| 10–20 | 0.76 ± 0.06 | 0.71 ± 0.10 | .261 | ||
| 20–30 | 0.63 ± 0.081 | 0.57 ± 0.066 | .120 | ||
| Central division | |||||
| Right intercostal | |||||
| 10–20 | 0.64 ± 0.095 | 0.62 ± 0.099 | .739 | ||
| 20–30 | 0.54 ± 0.075 | 0.55 ± 0.067 | .622 | ||
| Subcostal | |||||
| 10–20 | 0.72 ± 0.100 | 0.69 ± 0.085 | .423 | ||
| 20–30 | 0.60 ± 0.065 | 0.59 ± 0.077 | .781 | ||
Box-and-whisker plots of attenuation coefficients (ACs) of the hepatic parenchyma in 10 healthy Beagles at scan depths of 10 to 20 mm and 20 to 30 mm (measured from the hepatic capsule). ACs measured at a depth of 20 to 30 mm from the liver capsule were significantly (*P < .01, †P < .001) less than those measured at a depth of 10 to 20 mm. In each plot, the box represents the interquartile (25th to 75th percentile) range, the horizontal line in the box represents the median, the x in the box represents the mean, and the whiskers represent the range.
Citation: American Journal of Veterinary Research 83, 8; 10.2460/ajvr.21.11.0194
Box-and-whisker plots of attenuation coefficients (ACs) of the hepatic parenchyma in 10 healthy Beagles measured via the left intercostal, subcostal, and right intercostal approaches. The ACs measured via the subcostal approach were significantly (*P < .01, †P < .001, ‡P < .05) greater than those measured via the left intercostal and right intercostal approaches.
Citation: American Journal of Veterinary Research 83, 8; 10.2460/ajvr.21.11.0194
There was no significant difference (P = .166) between the ACs measured during the free-breathing and breath-holding conditions. The mean ± SD AC while dogs were breathing freely was 0.68 ± 0.086 dB/cm/MHz (range, 0.56 to 0.84 dB/cm/MHz), and the mean ± SD AC during the breath-holding condition was 0.65 ± 0.080 dB/cm/MHz (range, 0.53 to 0.78 dB/cm/MHz).
Repeatability of ATI
Intraday and interday examinations had good repeatability (ICC = 0.799 and 0.771, respectively; P < .001 for both; Table 2). Repeatability was good for both measurement sites (left and central divisions), both scanning planes (transverse and sagittal), a scanning depth of 10 to 20 mm from the liver capsule, and the right intercostal approach (P < .001 for all). Repeatability was moderate for a scanning depth of 20 to 30 mm from the liver capsule and the left intercostal and subcostal approaches (P < .001 for all). Only the central division was measured with the right intercostal approach. Scanning via the right intercostal approach at a depth of 10 to 20 mm showed good reliability. The mean ± SD AC measured at the central division of the liver via the right intercostal approach at a depth of 10 to 20 mm was 0.61 ± 0.054 dB/cm/MHz (range, 0.53 to 0.73 dB/cm/MHz).
Intraclass correlation coefficients (ICCs) associated with measurement of attenuation coefficients of the hepatic parenchyma in 10 healthy Beagles.
| Factor | Levels | ICC | ICC (95% CI) | P value |
|---|---|---|---|---|
| Intraobserver | ||||
| Intraday | 0.799 | 0.740–0.844 | < .001 | |
| Interday | 0.771 | 0.678–0.834 | < .001 | |
| Scanning plane | ||||
| Transverse | 0.755 | 0.648–0.830 | < .001 | |
| Sagittal | 0.840 | 0.770–0.889 | < .001 | |
| Measurement site | ||||
| Left division | 0.778 | 0.680–0.846 | < .001 | |
| Central division | 0.817 | 0.737–0.873 | < .001 | |
| Scanning depth (mm) | ||||
| 10–20 | 0.764 | 0.633–0.849 | < .001 | |
| 20–30 | 0.686 | 0.506–0.801 | < .001 | |
| Scanning approach | ||||
| Left intercostal | 0.725 | 0.535–0.837 | < .001 | |
| Subcostal | 0.738 | 0.624–0.818 | < .001 | |
| Right intercostal | 0.870 | 0.782–0.922 | < .001 |
Discussion
Our study evaluated technical factors influencing the ACs obtained by means of ATI (scanning plane, measurement site, scanning depth, scanning approach, and breathing condition) and the repeatability of ATI—an ultrasound-based technique for evaluating the attenuation of parenchymal organs quantitatively.20,22 We found that the ACs were not influenced by the measurement site, scanning plane, or breathing condition, but varied according to the scanning depth and scanning approach.
Some previous studies1,9–11,28 in veterinary medicine evaluated diffuse hepatic disease quantitatively with histogram and echo signal analyses. In the case of histograms, the intensity is obtained by presenting a graphical distribution of the pixel intensity of the ROI on the digitized grayscale image. In contrast, with ATI, the intensity is measured from the ultrasound beam with a specific transmission and reception sequence.12,29 For echo signal analysis, the echo signal obtained from the B-mode image of the dog’s liver and the reference phantom are digitized and analyzed with image analysis software. The echo value of the liver is compared to the echo value of the reference phantom and is expressed as the relative echo value to obtain the attenuation value of the liver.9–11 In contrast, the ACs can be acquired in real time with ATI without the need for further processing or reference phantom analysis.
In our study, AC values were significantly less in the deeper fields than in the near fields. According to the previously mentioned formula, the AC is inversely proportional to the distance traveled by the sound wave and is proportional to the intensity of the sound wave. The intensity decreases exponentially with the distance traveled, as shown by the formula I = I0e−2αz, where I0 is the intensity at z = 0 (measured in decibels), α is the pressure frequency-dependent attenuation coefficient per centimeter, and z is depth (measured in centimeters).17 Therefore, when the sound wave travels a greater distance, its intensity reduces, which results in a decrease in the AC value. Hence, we assumed that AC values decreased with an increase in the scanning depth.
The AC values acquired via the subcostal approach were significantly greater than those acquired via the left and right intercostal approaches in our study. From the perspective of ultrasound physics, attenuation is affected mainly by absorption, scattering, and reflection. The absorption of ultrasound waves is affected by the viscosity of the medium, relaxation time of the medium, and beam frequency. In soft tissues, the absorption of ultrasound waves increases in direct proportion to the beam frequency.15 Because the frequency of the ultrasound beam was fixed in our study, the different scanning approaches may not have affected the extent of absorption. Scattering also increases in proportion with frequency raised to the power of 4 and is independent on the incident angle.16 Thus, the different scanning approaches may not have affected the extent of scattering, similar to absorption, and for the same reason that the frequency was fixed. On the other hand, the reflection generated at the liver capsule possibly caused the difference in intensity of the transmitted wave between the intercostal and subcostal approaches. The degree of reflection is determined by the angle of incidence, and the intensity of the reflection is greater at a normal incidence (90° to the surface of the boundary) than that at an oblique incidence.16,30 With the intercostal approach, the transducer was perpendicular to the skin and liver capsule, but it was oblique to the liver capsule with the subcostal approach because scanning was performed at an angle of 30° to 45° to the abdominal surface of the dog. Accordingly, the reflected sound waves may have been decreased, and the transmitted sound waves might have been increased, with the subcostal approach compared with the intercostal approach, resulting in the ACs being greater with the subcostal approach than with the intercostal approach. Because the intensity of transmittance may vary with incident angle during examinations, scanning with the intercostal approach with the transducer perpendicular to the skin is recommended.
The ACs were not affected by the breathing condition in our study. In human studies,12,19,20,24–26 examination protocols include having patients hold their breath for approximately 3 to 5 seconds during AC acquisition. In contrast, results of our study showed that sedation or breath-holding was not necessary to minimize respiration-induced movement of the liver in dogs. Thus, high clinical applicability is expected, because ATI is easy to use, even in patients with low compliance.
The assessment of intraday and interday reliability of ATI measurements showed that measurements were repeatable, regardless of the measurement site or scanning plane. Previous human studies13,24 that evaluated the intraobserver reliability of ATI found that the reliability was excellent regardless of sex, age, body mass index, skin-to-liver capsule distance, or chronic hepatic disease. On the other hand, although the repeatability was good at a measuring depth of 10 to 20 mm in our study, it decreased at a depth of 20 to 30 mm. This was consistent with the result of a human study,22 which found that diagnostic accuracy decreased with an increase in depth from the surface. As for the scanning approach, only the right intercostal approach showed good repeatability, whereas the left intercostal and subcostal approaches showed moderate repeatability. Although all dogs were fasted to limit variations in liver evaluation resulting from gastric dilatation, the amount of gastric gas could have been different in each dog. Because the system cannot differentiate between attenuation of fat content and reverberation artifacts, it is assumed that the interference of various degrees of reverberation artifacts in the left intercostal approach caused fluctuations in measured ACs, resulting in low repeatability.25 As stated previously, low repeatability with the subcostal approach seemed to be the result of scanning angle.
There were several limitations to our study. First, it did not assess interobserver reproducibility. However, some human studies22,24 showed that ATI measurements have good interobserver reliability. Second, cytologic and histologic assessment of the liver was not conducted, and the liver was assumed to be normal on the basis of results of a physical examination, CBC, serum biochemical panel, radiography, abdominal ultrasonography, and echocardiography. Third, the dogs ranged from 1 to 9 years in age. However, as mentioned earlier, 2 human studies22,24 revealed that reliability was not influenced by the age of the participants. Fourth, the evaluation of breath-holding was not conducted with all measurement conditions, and further studies assessing variations associated with breathing condition are needed to confirm the results of our study. Last, ATI involves manufacturer-specific software, which can limit the generalizability of its application.
In conclusion, ATI was found to be a feasible technique for evaluating the hepatic parenchyma in healthy dogs. It also showed good intraoperator repeatability and was not influenced by the scanning plane, measurement site, or breathing condition. Scanning the central division of the liver via the right intercostal approach at a depth of 10 to 20 mm was found to be reliable and may be a useful examination protocol. ATI could be a useful diagnostic tool for evaluating diffuse hepatic disease in clinical veterinary medicine when used in conjunction with cytologic or histologic evaluation. Our study provided basic data for the use of ATI in veterinary patients, and further investigations are needed to evaluate the diagnostic performance of ATI for detecting vacuolar hepatopathy in dogs and cats.
Acknowledgments
The authors thank Canon Medical Systems Korea and Roy Park for equipment support and technical assistance with the ATI system. The authors declare there are no conflicts of interest.
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