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Keywords:

  • computed tomography;
  • dog;
  • hepatic metastatic tumor;
  • hepatocellular carcinoma;
  • nodular hyperplasia

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

The purpose of this study was to determine the utility of triple-phase helical computed tomography (CT) for differentiating canine hepatic masses. Seventy dogs with hepatic masses underwent triple-phase CT followed by surgical removal of the hepatic masses. Triple-phase helical CT scans for each dog included precontrast, arterial phase, portal venous phase, and delayed phase studies. The removed hepatic masses were histopathologically classified as hepatocellular carcinoma (n = 47), nodular hyperplasia (n = 14), and hepatic metastatic tumors (n = 9) in dogs. Of the 47 hepatocellular carcinomas, the most common CT findings included a heterogeneous pattern with hyper-, iso-, and hypoenhancement in both the arterial and portal venous phases (40/47, 85.1%). Of the 14 nodular hyperplasias, the most common CT findings were a homogeneous pattern with hyper- and isoenhancement in both the portal venous and delayed phases (13/14, 92.9%). Of nine hepatic metastatic tumors, the most common CT findings included a homogeneous hypoenhancement pattern in both the arterial and portal venous phases (8/9, 88.9%). In addition, 5 (55.6%) showed homogeneous hypoenhancement patterns in the delayed phase. Findings from our study indicated that triple-phase CT is a useful tool for preoperative differentiation of hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic tumors in dogs.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

Helical computed tomography (CT) allows images of the entire liver to be obtained during the phase of maximum parenchymal enhancement, enabling optimal detection of focal hepatic lesions.[1] Accurate diagnosis is critical in patients with hepatocellular carcinoma (HCC), hepatic metastatic tumors, or nodular hyperplasia (NH) because they are possible candidates for surgical treatment and the tumors have radically different prognoses.[2] Dynamic CT may be useful for distinguishing between benign and malignant neoplasms in humans[3, 4] and dogs.[5, 6]

Development of multidetector helical CT (MDCT) ensured that dynamic CT could be used to evaluate the hemodynamics of hepatic masses and that triple-phase helical CT could be used to rapidly scan the whole abdomen in three phases. In triple-phase helical CT, a single bolus injection facilitates imaging during the phase of preferential arterial enhancement, that is, the arterial phase, followed by the portal venous phase and delayed phase.[7] In humans, previous studies have shown that triple-phase helical CT improves the detection of various hepatic masses.[7-10] In addition, three-dimensional (3D) reconstruction of triple-phase helical CT would be useful for preoperative planning.[11]

To the best of our knowledge, however, there have been no reports on the triple-phase CT characteristics of for various hepatic masses in dogs. We believe that, as in humans, triple-phase helical CT is a convenient and less invasive method for the differential diagnosis of hepatic masses and preoperative planning in dogs. The purpose of this study was to characterize triple-phase helical CT findings in dogs with naturally occurring hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic tumors.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

Animals

Privately owned dogs referred to the Animal Medical Center of Nihon University for suspected hepatic masses were prospectively recruited. For all dogs, suspected hepatic masses were based on abdominal radiography and ultrasonography (US) findings. With informed owner consent, the dogs underwent triple-phase helical CT, followed by surgical removal of the hepatic masses. The resected masses were histopathologically diagnosed by Hematoxylin-Eosin staining by one pathologist (Y. K.). The cases with hepatic masses diagnosed as hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic tumors were selected for image analysis.

Triple-Phase Helical CT technique

In all dogs, an 18–27 G over-the-needle catheter was placed in the cephalic vein. Each dog was premedicated with midazolam hydrochloride (0.2 mg/kg, intravenously) and butorphanol tartrate (0.2 mg/kg, intravenously) and intubated after induction with intravenous propofol. General anesthesia was maintained by mechanical ventilation with isoflurane (1.5–2%) and oxygen (2 l/min). All dogs were positioned in ventral recumbency, and all scans were obtained on a 16 MDCT scanner (Aquilion 16; Toshiba Medical Systems, Otawara, Japan). The scanning parameters were as follows: rotation time, 0.5 s; slice thickness, 1–2 mm; reconstruction interval, 0.5–1 mm; table speed, 16–32 mm/rotation; helical pitch, 16.0; X-ray tube potential, 120 kV; and X-ray tube current, 150 mA. All helical scans were started at the tip of the wing of the ilium in a cranial direction and covered the entire liver. Iohexol (Ioverin 300; Teva Pharma Japan Inc., Nagoya, Japan) was used as a contrast medium and was administered at a dose of 2.5 ml/kg (750 mgI/kg) via the cephalic vein with a power injector (Auto Enhance A-60; Nemoto-Kyorindo, Tokyo, Japan). The injection time was 15–20 s (injection speed, 0.3–3 ml/s) as described previously.[5, 12] In cases where the injection speed was calculated to exceed 3 ml/s the injection time of the contrast medium would have to be within 20 s, and so the injection speed was fixed at 3 ml/s (the range of injection time was 21–31 s). Precontrast (before the injection of contrast medium), arterial phase (20 s after the start of injection of the contrast medium), portal venous phase (40 s after the start of the injection), and delayed phase (120 s after the start of the injection) scans were obtained. The scanning time for each phase was approximately 8 s. In all dogs, 3D images were reconstructed from the obtained images on a workstation after scanning (AZE Virtual Place Plus; AZE, Tokyo, Japan).

Image Analysis

All CT images were reviewed on a dedicated computer workstation. The size (largest transverse dimension) and location of the lesion were recorded. The contrast values were recorded as Hounsfield Units (HU). The contrast value of mass enhancement was measured using the most visually enhanced portion of the mass. In cases with two or more masses, the largest tumor was analyzed. For comparative purposes, the contrast values in three portions of the normal hepatic parenchyma adjacent to the mass were measured, and the mean value was calculated as the contrast value of hepatic parenchyma. An attempt was made to maintain a region-of-interest (ROI) area of approximately 30 mm2 for all measurements of contrast values. Hyperenhancement was defined as a mass contrast value at least 10 HU greater than the hepatic parenchyma contrast value. Isoenhancement was defined as a mass contrast value was that was greater or less than the hepatic parenchyma contrast value by <10 HU, and hypoenhancement was defined as a mass contrast value at least 10 HU less than the hepatic parenchyma contrast value. Further, each lesion was judged to have homogeneous or heterogeneous enhancement in each phase as described previously.[2] Homogeneous and heterogeneous lesions were scored as being hypo-, iso-, or hyperenhanced.

Data Analysis

Statistical tests were performed using commercially available statistical analysis software (Stat Mate III; ATMs. Co, Tokyo, Japan). Data on the hepatic mass and parenchyma contrast values, body weight, mass size, and injection time and speed were represented as mean ± standard deviation. Spearman's rank test was used to analyze relationships among all of the contrast values and body weight, mass size, and the injection time and speed of the contrast medium. The Mann–Whitney U-test was used to compare hepatic parenchyma and mass contrast values. The contrast enhancement patterns were analyzed by a Chi-square test, followed by Yates post hoc correction test. Body weight, injection speed, the size and number of masses, and the contrast values were statistically compared for all mass types using the Kruskal–Wallis H-test. The relationship between mass size and contrast-enhancement pattern was also analyzed using the Kruskal–Wallis H-test. A P value less than 0.05 was considered to indicate a statistically significant difference.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

A total of 70 dogs were included in the study. Of the 70 dogs (30 males and 40 females; age, 7–16 years) with hepatic masses, 47, 14, and 9 dogs, were diagnosed with hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic masses, respectively. The nine metastatic masses were derived from seven splenic hemangiosarcomas, one splenic melanoma, and one intestinal undifferentiated sarcoma. The breeds were as follows: 12 mongrels, 10 Shih Tzus, 8 Golden Retrievers, 5 Beagles, 5 Miniature Dachshunds, 5 Shibas, 4 Labrador Retrievers, 4 Shetland Sheepdogs, 3 Chihuahuas, 2 Maltese dogs, 2 Pembroke Welsh Corgis, 2 Siberian Huskies, 2 Yorkshire Terriers, 1 American Cocker Spaniel, 1 Border Collie, 1 Flat-coated Retriever, 1 Pointer, 1 Pomeranian, and 1 Toy Poodle. The mean body weight of the dogs was 14.8 ± 9.1 kg, and the mean mass size (largest axial dimension) was 63.5 ± 33.2 mm. The mean size (largest axial dimension) of the hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic tumor masses was 75.7 ± 26.0, 47.0 ± 31.9, and 20.2 ± 20.4 mm, respectively. The injection speed was 2.0 ± 1.0 ml/s in all dogs. There was no statistical difference in weight/injection speed among mass types. The mean number of hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic tumor masses was 1.44 ± 0.9 (range: 1–5), 1.57 ± 0.75 (range: 1–3), and 4.77 ± 5.66 (range: 1–16), respectively. As for metastatic tumors, three dogs had more than five masses, whereas six patients had 1–3 masses. The number of hepatic masses was not significantly different among mass types.

The contrast values of the hepatic masses and parenchyma in each phase are summarized in Table 1. For all dogs, the contrast values of the hepatic masses and parenchyma were 100.3 ± 38.8 and 93.9 ± 20.7 HU in the arterial phase, 123.0 ± 43.1 and 137.9 ± 15.9 HU in the portal venous phase, and 106.3 ± 30.1 and 121.7 ± 11.8 HU in the delayed phase, respectively. None of the contrast values was significantly correlated with body weight, mass size, or injection speed. For the hepatocellular carcinomas, the contrast values of the hepatic masses were significantly lower than those of the parenchyma in the portal venous and delayed phases. For the hepatic nodular hyperplasias, the contrast values of the hepatic masses were significantly higher than those of the parenchyma in the arterial phase. For the hepatic metastatic tumors, the contrast values of the hepatic masses were significantly lower than those of the parenchyma in all phases. Moreover, the contrast values of hepatic metastatic tumors were significantly lower than those of the other masses in the arterial and portal venous phases. The contrast values of the hepatic nodular hyperplasias were significantly higher than those of the other masses in the portal venous and delayed phases.

Table 1. Mean Contrast Values of Hepatic Masses and Surrounding Liver Parenchyma as Seen in 70 Patients on Triple-Phase CT
  APPVPDP
TypenMassParenchymaMassParenchymaMassParenchyma
  1. The contrast value is the Hounsfield Unit (HU). All data are mean ± SD.

  2. *AP, arterial phase; DP, delayed phase; HCC, hepatocellular carcinoma; NH, nodular hyperplasia; PVP, portal venous phase, HU of masses were significantly lower than that of liver parenchyma, HU of masses were significantly higher than that of liver parenchyma, *HU of masses were significantly higher than that of the other masses, **HU of masses were significantly lower than that of the other masses.

Total70100.3 ± 38.893.9 ± 20.7123.0 ± 43.1137.9 ± 15.9106.3 ± 30.1121.7 ± 11.8
HCC47102.7 ± 40.394.0 ± 21.3120.9 ± 43.6138.9 ± 16.2104.6 ± 30.3122.2 ± 9.4
NH14111.6 ± 30.3‡*90.4 ± 17.5155.6 ± 25.7*137.2 ± 18.2126.2 ± 16.6122.1 ± 15.3
Metastatic tumor965.6 ± 20.994.4 ± 21.083.2 ± 24.8†**133.8 ± 11.684.4 ± 31.1†**119.4 ± 17.9

Three-dimensional reconstruction images were created for all dogs. The 3D images were helpful for visualizing the spatial relationships among the masses, liver parenchyma, and intra-abdominal vessels, including the caudal vena cava, portal vein, and hepatic artery and vein (Fig. 1). The contrast-enhancement patterns of all of the hepatic masses are summarized in Table 2. For the hepatocellular carcinomas, the most common contrast-enhancement pattern was heterogeneous enhancement in the arterial phase (85.1%), portal venous phase (85.1%), and delayed phase (66%) (Fig. 2), which was significantly different compared with those of the other masses. For the hepatic nodular hyperplasias, the most common contrast-enhancement pattern was homogeneous hyper- and isoenhancement in the arterial phase (57.1%), portal venous phase (92.9%), and delayed phase (92.9%; Figs. 3 and 4), which was also significantly different compared with the other masses. For hepatic metastatic tumors, the most common contrast-enhancement pattern was homogeneous hypoenhancement in the arterial phase (100%) and portal venous phase (88.9%). In addition, a homogeneous pattern was seen in all phases, and hypoenhancement was observed in 100% of the arterial phase images and 88.9% of the portal venous phase images. As for the delayed phase images, 44.4% and 55.6%, respectively, showed iso- and hypoenhancement (Figs. 5 and 6). For the metastatic tumors, the most common contrast-enhancement pattern was significantly different from that of the other masses. There was no significant association between contrast-enhancement pattern and mass size.

image

Figure 1. Three-dimensional (3D) images created using triple phase CT in a dog with hepatocellular carcinoma. The imaging angle is the left dorsal direction. (A) Three-dimensional image in the arterial phase. The brown portion is the liver parenchyma. The green portion is the tumor and the red portion is the aorta and left kidney. Hepatic carcinoma originated from the caudate and right lateral lobes. (B) Three-dimensional image with the liver parenchyma removed in the arterial phase. Arrow: vessel involved in the tumor. (C) Three-dimensional image in the portal venous phase. The blue portions are the veins and left kidney. The purple portion is the portal vein. Arrow: vessel involved in the tumor.

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Table 2. Enhancement Features of Hepatic Masses as Seen in 70 Patients on Triple-phase CT
  Enhancement patternAPPVPDP
TypenContrastEnhancementn%n%n%
  1. AP, arterial phase; DP, delayed phase; HCC, hepatocellular carcinoma; NH, nodular hyperplasia; PVP, portal venous phase. significantly larger compared with the other groups.

HCC47Homogeneous 714.9714.91634
   Hyper36.412.148.5
   Iso0012.1612.8
   Hypo48.5510.6612.8
  Heterogeneous 4085.14085.13166
   Hyper2144.7817.136.4
   Iso919.11327.61225.5
   Hypo1021.31940.41634
          
NH14Homogeneous 857.11392.91392.9
   Hyper642.9857.2321.5
   Iso214.3535.71071.4
   Hypo000000
  Heterogeneous 642.917.117.1
   Hyper428.617.117.1
   Iso000000
   Hypo214.20000
          
Metastasic tumor9Homogeneous 9†10091009100
   Hyper000000
   Iso00111.1444.4
   Hypo9100888.9555.6
  Heterogeneous 000000
   Hyper000000
   Iso000000
   Hypo000000
image

Figure 2. Triple phase CT characteristics in a dog with hepatocellular carcinoma. (A) Transverse precontrast CT image showing a tumor in the right lobe. (B) Heterogeneous tumor enhancement in the arterial phase. (C) Heterogeneous enhancement in the portal venous phase. (D) Heterogeneous enhancement in the delayed phase. Black arrow head: aorta. White arrow head: portal vein.

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image

Figure 3. Triple phase CT characteristics in a dog with nodular hyperplasia. (A) Transverse precontrast CT image showing a mass in the left lobe (arrow). (B) Heterogeneous enhancement in the arterial phase. (C) Homogeneous hyperenhancement in the portal venous phase. (D) Homogeneous isoenhancement in the delayed phase. White arrow: mass. Black arrow head: aorta. White arrow head portal vein.

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image

Figure 4. Triple phase CT characteristics in a dog with nodular hyperplasia. (A) Transverse precontrast CT image showing a mass in the right lobe. (B) Heterogeneous enhancement in the arterial phase. (C) Homogeneous isoenhancement in the portal venous phase. (D) Homogeneous isoenhancement in the delayed phase. Black arrow head: aorta. White arrow head: portal vein.

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image

Figure 5. Triple phase CT characteristics in a dog with a hepatic metastatic tumor. (A) Transverse precontrast CT image showing a mass in the right lobe (arrow). (B) Homogeneous tumor hypoenhancement in the arterial phase. (C) Homogeneous hypoenhancement in the portal venous phase. (D) Homogeneous hypoenhancement in the delayed phase. White arrow: tumor. Black arrow head: aorta. White arrow head: portal vein.

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image

Figure 6. Triple phase CT characteristics in a dog with a hepatic metastatic tumor. (A) Transverse precontrast CT image showing a mass in the right lobe (arrow). (B) Homogeneous tumor hypoenhancement in the arterial phase. (C) Homogeneous hypoenhancement in the portal venous phase. (D) Homogeneous isoenhancement in the delayed phase. White arrow: tumor

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

In the current study, body weight and the injection speed were found to have no significant correlations with any of the hepatic parenchyma and mass contrast values. The entire liver was evaluated in one examination with triple-phase helical CT and multiple masses were detected. Three-dimensional reconstruction images showing the detailed morphological features of the canine intra-abdominal structures were also obtained. In addition, the 3D reconstruction imaging techniques helped to identify vascular involvement. A previous study reported that evaluation of enhancement patterns in dynamic CT may be helpful in the differentiation of hepatocellular carcinoma and hepatic nodular hyperplasia in dogs.[5], [6] However, in dynamic CT, hepatic masses must be first detected in the precontrast images because the ROI is placed on a predetermined slice for the dynamic scan. In the case of multiple hepatic masses, multiple dynamic scans are required to evaluate the enhancement of different masses. Other previous studies have reported differentiation of hepatic tumors using contrast enhanced US,[13-15] and identified a high diagnostic yield for hepatic masses. However, the field of view for acquiring contrast enhanced US images must be limited to a small focal area and this area must be subjectively selected by the operator.

In our study, CT findings of hepatocellular carcinoma were typically heterogeneous in the arterial and portal venous phases in dogs. In a previous study performed using dual-phase helical CT (arterial and portal venous phases) in human subjects, the most common enhancement pattern in hepatocellular carcinoma was heterogeneous in the

arterial phase (sensitivity, 60%; specificity, 96%; PPV, 75%)[2] but masses were not identifiable on the portal venous phase images. In dogs with hepatocellular carcinoma, the heterogeneous contrast pattern observed in our study was similar to that observed in previous studies using dynamic CT.[5, 6] In these studies,[5, 6] hepatocellular carcinoma showed hypoenhancement in the delayed phase. In our study, the average contrast value of the hepatocellular carcinoma was lower than that of the liver parenchyma in the delayed phase. However, just 46% (22/46) of hepatocellular carcinomas showed hypoenhancement in the delayed phase, and the enhancement patterns of hepatocellular carcinoma were comparatively variable. Therefore, evaluation of enhancement based on HU alone risks a misleading differential diagnosis of hepatocellular carcinoma in dogs. CT imaging criteria for hepatocellular carcinoma in humans are based exclusively on the vascular-dynamic findings of hepatocellular carcinoma with Iohexol. A typical enhancement is defined as an early arterial uptake followed by washout in the portal venous or late, delayed phase.[16] In humans, the enhancement pattern of hepatocellular carcinoma is affected by mass size and cellular differentiation.[16-18] In our study, however, the characteristic CT findings of hepatocellular carcinoma were not affected by multiphase enhancement or by tumor size. It is suggested that the vascular dynamics of hepatocellular carcinoma in dogs differs from that in humans. In our study, cellular differentiation and angiogenesis of hepatocellular carcinoma were not investigated. Clarification of the association between pathological changes and contrast-enhancement patterns may be required.

The most common CT findings for dogs with nodular hyperplasia in the present study were a homogeneous pattern and hyper- and isoenhancement in the portal venous and delayed phases. The finding of hyper- and isoenhancement of hepatic nodular hyperplasia in our study is similar to that reported in a previous study,[5] but different from the findings of another study where only isoenhancement in hepatic nodular hyperplasia was reported in dogs.[6] In a dual-phase helical CT study of human subjects, the most common enhancement pattern in nodular hyperplasia was homogeneous hyperenhancement in the portal venous phase (sensitivity, 70%; specificity, 88%; PPV, 61%) and homogeneous isoenhancement in the portal venous phase (sensitivity, 40%; specificity, 96%; PPV, 73%).[2] It is suggested that the morphologic characteristics of nodular hyperplasia in dogs closely resemble the histologic architecture of nodular hyperplasia in humans. The homogeneous finding is most likely related to the rarity of hemorrhage and necrosis in nodular hyperplasia in dogs.

In the present study, the most common CT findings in dogs with hepatic metastatic tumors were homogeneous hypoenhancement in the arterial and portal venous phases. A previous study in dogs reported that hypoattenuating lesions within the hepatic parenchyma in postbolus contrast CT (similar to the delayed phase) were probable hepatic metastatic tumors (sensitivity, 73%; specificity, 79%; PPV, 73%).[19] In the delayed phase in our study, 44.4% of the hepatic metastatic tumors showed isoenhancement and 55.6% hypoenhancement. It is suggested that the use of triple-phase helical CT may significantly improve the detection rate of hepatic metastatic tumors.

In conclusion, the most common CT characteristics of hepatocellular carcinoma included a heterogeneous pattern with hyper-, iso-, and hypoenhancement in both arterial and portal venous phases. The most common CT characteristics of nodular hyperplasia were a homogeneous pattern with hyper- and isoenhancement in both the portal venous and delayed phases. The most common CT characteristics of metastatic tumors included a homogeneous hypoenhancement pattern in both the arterial and portal venous phases. Findings from our study indicated that triple-phase helical CT is a useful tool for preoperative differentiation of hepatocellular carcinoma, nodular hyperplasia, and hepatic metastatic tumors based on images in dogs. Large-scale studies are needed in order to determine the diagnostic sensitivity and specificity of triple-phase helical CT characteristics for predicting histopathologic classification of hepatic masses in dogs.

REFERENCES

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES
  • 1
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    Irausquin RA, Scavelli TD, Corti L, et al. Comparative evaluation of the liver in dogs with a splenic mass by using ultrasonography and contrast-enhanced computed tomography. Can Vet J 2008;49:4652.