Ultrasonographic characteristics of the portal venous system of 37 healthy, unsedated, student-owned cats: A prospective study

Abstract

Objective

The aim of this study was to determine portal vein and divisional branch diameters and portal vein velocities in healthy, unsedated cats, using B-mode and Doppler ultrasound.

Animal

Thirty-seven healthy, adult cats, all owned by students.

Procedure

Enrollment of cats in the study was done prospectively. Ultrasonographic imaging in both the longitudinal and transverse planes was assessed, with all examinations and measurements done by the same person. The assessment included the following 3 sites: extra-hepatic portion of the portal vein, intra-hepatic branches of the portal vein, and the aorta at the level of the porta hepatis. The Shapiro-Wilk test was used for normality and P < 0.05 was used to define statistical significance.

Results

Both the extra-hepatic portion of the portal vein and the porta hepatis were identified in all 37 cats (100%), whereas the aorta was recorded in 31 (84%), and the left and right intra-hepatic branches of the portal vein were seen in 29 (78%). Pulsed-wave Doppler ultrasound of the portal vein was obtained in 32 cats (86%). In longitudinal view, average maximal diameter of the extra-hepatic portal vein was 3.6 mm (± 0.7 mm), and the mean portal flow velocity was 14.6 cm/s (± 4.3 cm/s). In transverse view, average maximal diameter was 4.8 mm (± 0.8 mm) for the extra-hepatic portal vein, and 3.1 mm (± 0.8 mm) and 2.6 mm (± 0.7 mm) for the left and right intra-hepatic branches, respectively. The portal-vein-to-aorta ratio averaged 1.2 (± 0.2).

Conclusion

This study produced sonographic data of the portal venous system in healthy, conscious adult cats, which may be useful during investigation of liver diseases, including congenital and acquired liver diseases.

Introduction

The normal liver has a dual blood supply, deriving 70 to 80% of its blood from the portal vein and the remainder from the hepatic artery. The portal vein is formed by the confluence of the cranial and caudal mesenteric veins, along with the splenic vein in dogs and cats and the gastroduodenal vein in dogs. After entering the liver, the portal vein divides into the left and right branches (1). In cats, hepatobiliary diseases have been extensively described and can be separated into various categories, such as inflammatory, infectious, vascular, metabolic, toxic, neoplastic, and biliary diseases (2–7). Although liver sampling may provide a definitive diagnosis, with an overall agreement between cytologic and histologic diagnosis ranging from 51 to 61% (8,9), some hepatic vascular anomalies can be diagnosed with non-invasive diagnostic imaging techniques (4).

Computed tomographic angiography (CTA) is the gold standard for evaluating the portal venous system in human and veterinary medicine (10–12). It is non-invasive, fast, and generates images of all portal tributaries and branches. However, CTA is expensive and requires heavy sedation or general anesthesia which can be a limiting factor for animal owners. Furthermore, CTA also requires contrast media injection which requires appropriate kidney function; that can be limiting in young patients or those with kidney disease.

Ultrasound is a non-invasive, widely available modality that does not require the use of general anesthesia, special licensing, or hazardous agents (4). This modality can be helpful in the diagnosis of hepatic vascular anomalies in feline patients and can provide information on flow dynamics that can be used in the follow-up of treated patients (3,6,13–20). Portosystemic shunts are rare and tend to be extrahepatic in cats; Persian, Siamese, Himalayan, and Burmese seem to be overrepresented breeds (15,21). Based on operator experience, sensitivity of ultrasonography for detection of portosystemic shunts in cats varied from 80 to 92%, and specificity varied from 67 to 98%, when compared to surgical, portographic, or necropsy findings, and depended on the etiology (congenital or acquired) and location (extra- or intra-hepatic) of the shunt (16,18).

Accurate ultrasonographic assessment requires a thorough understanding of the portal vascular system anatomy, as well as color and spectral Doppler tools. To our knowledge, there is limited information regarding normal sonographic values of the portal venous system in the feline population. The purpose of this study was to collect sonographic characteristics of the terminal portion of the portal vein and intra-hepatic divisions using conventional and Doppler ultrasound in healthy, unsedated adult cats owned by students. We hypothesized that ultrasonography can be used to evaluate portal vein diameters and blood velocities in a healthy, unsedated, population of cats.

Materials and methods

This prospective descriptive study was conducted at the Veterinary Medical Center of the National Veterinary School of Toulouse, from June 2017 to March 2018. In preliminary work, the investigators used 1 of their own cats to establish a standardized protocol and help inform the study design. The study protocol was approved by an ethics committee and established internationally recognized high standards of veterinary clinical care for each individual patient were always followed. Participation in the study was voluntary and a written informed consent was obtained from the owner of all cats used. Inclusion criteria included healthy student-owned cats, > 6 mo of age, with complete medical history and medical records. All cats were considered healthy based on their medical history and physical examination. Owners were asked to withhold food the night before the procedure. Cats were scanned consciously; no chemical restraint was used. Any cat that was too stressed to tolerate a non-sedated ultrasound scan was excluded from the study. In addition, poor quality ultrasonographic images that prevented an accurate measurement of portal vasculature were also excluded.

One author (CLL) with 20 y of experience performed all the ultrasound scans; the other author (MD) was responsible for getting a complete history and analyzing the data. During the examination, efforts were made to minimize patient stress. Each cat was positioned in dorsal recumbency in a dedicated bed, and 1 or 2 assistants helped hold the cat during the scan. To reduce stress for the cat, the abdomen was not clipped, but it was made wet with warm water, and ultrasound gel was generously applied to improve image quality. Each cat was given a specific case number and each image was labeled and recorded. During the preliminary work, the smaller footprint of the microconvex transducer was preferred over a linear transducer. For every procedure, ultrasonographic recordings were obtained using the same ultrasound machine (Philips EPIQ 5 ND, Philips Healthcare) and a multifrequency microconvex curvilinear (5–8 MHz) transducer.

A standardized ultrasound protocol was used for each cat. To locate the porta hepatis, the transducer was placed in a longitudinal plane, caudal to the ribs. Images were considered adequate when artifacts, such as gas or ingesta, did not impair proper visualization of vascular structures. First, the extrahepatic segment of the portal vein (PV) was identified in the cranial abdomen, at the level of the porta hepatis, ventrally to the caudal vena cava and the aorta. Three images of the PV were recorded in a longitudinal view. Then, the transducer was rotated 90° from the longitudinal view and 3 images of the PV were recorded in a transverse view (Figure 1). A special effort was made to reduce the pressure applied by the transducer on the abdomen while recording images.

Figure 1.

Longitudinal axis (LG) and transverse axis (TV) views of the portal vein at the level of the porta hepatis. PV — Portal vein. The plain white lines (A and B) represent portal vein diameter measurements, whereas the white arrow represents the portal vein at the level of the porta hepatis.

Second, color and pulsed-wave Doppler with B-mode duplex imaging were subsequently completed on the PV along the longitudinal plan. Effort was made to align the Doppler beam with the longitudinal axis of the extra-hepatic segment of the portal vein. The PV velocities were measured by placing the gate in the center of the vessel using pulsed-wave Doppler. The angle of insonation was measured with angle correction every time and was < 60° with respect to the flow within the gate (Figures 2, 3).

Figure 2.

Color flow Doppler image of the portal vein at the level of the porta hepatis on a longitudinal subxiphoid view. The plain white arrows represent the left and right intra-hepatic divisions of the portal vein (left portal branch in the near field). See Figure 1 for remainder of key.

Figure 3.

Pulsed-wave Doppler image of the portal vein at the level of the porta hepatis on a longitudinal subxiphoid view. A small Doppler sample volume was placed at the center of the portal vein (PV). Resulting velocity spectrum showing variable maximum velocity. Vertical axis is velocity in cm/s, whereas the white bar in the x-axis represents 1 s. See Figure 1 for remainder of key.

Third, the left and right intra-hepatic divisions of the PV (left and right portal branches) were evaluated, and 3 images of each were recorded in the transverse and longitudinal views. Last, a longitudinal view of the aorta at the level of the porta hepatis was evaluated and images were obtained. When cat compliance permitted, a transverse image of the aorta was also obtained.

All images were transferred to a postprocessing workstation, and the author (MD) performed measurements using specific software (Horos Project, GNU LGPL, Version 3.0). For each transverse image of the PV, intra-hepatic portal branches and aorta, the minimal and maximal diameters were obtained, and the portal vein area was calculated using the following formula for ellipsoid structures:

$$\text{PV\hspace{0.17em}area\hspace{0.17em}}({\text{cm}}^2)=\mathrm{\pi }\times \frac{\text{PV\hspace{0.17em}max\hspace{0.17em}diameter\hspace{0.17em}}(\text{cm})}{2}\times \frac{\text{PV\hspace{0.17em}min\hspace{0.17em}diameter\hspace{0.17em}}(\text{cm})}{2}$$

For each longitudinal image of the PV, intra-hepatic portal branches and aorta, 3 maximal diameters were measured, and an average calculated. Each measurement was made perpendicular to the wall of the vessel, inner edge to inner edge. The portal flow (PF), portal vein-to-aorta ratio (PV/Ao), pulsatility index (PI) and congestion index (CI) were subsequently calculated.

The mean portal velocity was obtained by multiplying the maximal velocity by the coefficient 0.57, as described (16), and the mean portal flow (PF) was measured using the following formula:

$$\text{PF\hspace{0.17em}}\hspace{0.17em}(\text{mL}/\text{min}/\text{kg})=\frac{\text{PV\hspace{0.17em}max\hspace{0.17em}velocity\hspace{0.17em}}(\text{cm}/\text{s})\times 0.57\times 60\hspace{0.17em}(\text{s}/\text{min})\times \text{PV\hspace{0.17em}area\hspace{0.17em}}({\text{cm}}^2)}{\text{Body\hspace{0.17em}weight\hspace{0.17em}}(\text{kg})}$$

The pulsatility index (PI) of the portal vein was calculated using the following formula:

$${\text{PI}}_{\text{PV}}=\frac{\text{PV\hspace{0.17em}max\hspace{0.17em}velocity\hspace{0.17em}}-\text{PV\hspace{0.17em}min\hspace{0.17em}velocity}}{\text{PV\hspace{0.17em}max\hspace{0.17em}velocity}}$$

The congestive index (CI) of the portal vein was calculated by using the following formula:

$${\text{CI}}_{\text{PV}}=\frac{\text{PV\hspace{0.17em}area}}{(\text{PV\hspace{0.17em}max\hspace{0.17em}velocity}\times 0.57)}$$

All statistical analyses were done with R software (Version 4.0.3; R Foundation for Statistical Computing, Vienna, Austria). The Shapiro-Wilk test was used to assess normality of distribution of continuous variables in our study sample. For P < 0.05, the null hypothesis (data were normally distributed) was rejected. Correlations were done between blood vessel dimensions and body weight or age; a Pearson’s correlation coefficient was used when normally distributed variables were evaluated, whereas a Spearman’s rank-order correlation coefficient was used when variables that were evaluated were not normally distributed. Outliers were detected using a Grubbs’ test and a ratio z of 1.96. For all analyses, P < 0.05 was used to define statistical significance.

Results

Thirty-seven cats were included in the study. There were 21 male cats, 17 of which were neutered. All 16 female cats were spayed. There were various breeds, including domestic short hair cats (n = 34), oriental breeds (n = 2), and 1 Maine coon. Age and body weight were normally distributed. The median age was 3.1 y (range: 0.5 to 7 y), and the median body weight was 4.5 kg (range: 2.9 to 7 kg).

The proportion of data collected during the study is presented in Table 1. For several cats, the author was unable to record all the images, due to patient movement during image acquisition. The porta hepatis and the extra-hepatic portion of the portal vein were identified in 37 cats (100%), the aorta was recorded in 31 cats (84%), and the left and right intra-hepatic branches of the portal vein were visualized in 29 cats (78%). Pulsed-wave Doppler ultrasound of the portal vein was obtained in 32 cats (86%). A laminar hepatopetal portal blood flow was identified at the level of the porta hepatis using color Doppler in all cats.

Table 1.

Proportion of data collected based on anatomical segment and ultrasonographic views (N = 37).

Recordings	Longitudinal view	Transverse view	Pulsed Doppler
Portal vein	37/37 (100%)	27/37 (73%)	32/37 (86%)
Right intra-hepatic portal division	29/37 (78%)	29/37 (78%)
Left intra-hepatic portal division	29/37 (78%)	29/37 (78%)
Aorta	31/37 (84%)	11/37 (30%)

The statistical distribution of the variables that were evaluated and their numerical values are reported in Table 2. Patient’s age and body weight were not significantly correlated with any variable.

Table 2.

Distribution of variables and numerical values associated with the study sample.

Vascular segment	Variable	n	Mean [± 1 SD] or median (Q1 to Q3)a
Extra-hepatic portal vein	Maximal diameter in transverse view (mm)	27	4.8 [4.0 to 5.5]
	Minimal diameter in transverse view (mm)a	27	3.5 (3.3 to 4.2)
	Maximal diameter in longitudinal view (mm)	37	3.6 [2.9 to 4.3]
	Maximal velocity (cm/s)	32	25.7 [18.1 to 33.3]
	Mean velocity (cm/s)	32	14.6 [10.3 to 19]
	Minimal velocity (cm/s)	32	9.2 [5.7 to 12.8]
	Portal flow (mL/kg/min)	23	29.9 [18.4 to 41.4]
	PV/Ao ratio	24	1.2 [1.0 to 1.4]
	Pulsatility indexa	32	0.65 (0.57 to 0.7)
	Congestive index (cm · s)	25	0.012 [0.006 to 0.017]
Right intra-hepatic portal division	Maximal diameter in transverse view (mm)	28	2.6 [1.9 to 3.2]
	Minimal diameter in transverse view (mm)	28	1.8 [1.3 to 2.4]
	Maximal diameter in longitudinal view (mm)a	29	1.4 (1.2 to 2.0)
Left intra-hepatic portal division	Maximal diameter in transverse view (mm)	29	3.1 [2.3 to 4.0]
	Minimal diameter in transverse view (mm)	29	2.1 [1.4 to 2.8]
	Maximal diameter in longitudinal view (mm)	29	2.0 [1.5 to 2.6]
Aorta	Maximal diameter in transverse view (mm)	11	4.1 [3.1 to 5.0]
	Minimal diameter in transverse view (mm)	11	3.6 [2.7 to 4.5]
	Maximal diameter in longitudinal view (mm)	31	3.9 [3.2 to 4.7]

^aVariables that are not normally distributed are expressed with medians and interquartile ranges in parenthesis.

n — Sample size; Q1 — First (lower) quartile; Q3 — Third (upper) quartile; SD — Standard deviation.

Discussion

The present study produced conventional and Doppler sonographic values for the main portal vein and the intra-hepatic portal branches of healthy, unsedated cats. The portal vein was easily visualized in all cats. Given their small size, the intrahepatic portal divisions were more difficult to record, particularly in restless or obese cats. Correlation analyses did not detect significant linear associations between age, body weight, and ultrasonographic characteristics of the portal vein. This finding supports a statement made in a previous report that the influence of body weight and age on the portal vein diameter and portal blood flow was minimal in the feline population (16).

In a retrospective study, a sub-group of cats with no portosystemic shunt had, in transverse view, a maximal portal vein diameter of 4.4 mm (n = 9) and a portal venous flow mean velocity of 17 cm/s (n = 5) (16). This was consistent with our results as the maximal portal vein diameter on transverse images was 4.8 mm (n = 27), and the portal venous flow mean velocity was 14.6 cm/s. In that same study, a portal vein-to-aorta ratio (PV/Ao) ≥ 0.8 consistently ruled out an extrahepatic portosystemic shunt, whereas a portal vein-to-aorta ratio ≤ 0.65 was consistently present in extrahepatic shunts. This was consistent with our results as the mean PV/Ao in our population was > 0.8. At the porta hepatitis, the portal vein divides into 2 divergent branches, and in dogs, the left branch is larger in diameter than the right (7,22). This anatomic finding was also reported in our feline population in which the maximal diameter of left branch was ~20% larger than the right branch. In cats, the left branch supplies more liver lobes (right medial lobe, papillary process, quadrate lobe, left medial, and left lateral lobes) than the right branch, consistent with its larger diameter.

In arteries and veins, the extracellular matrix constitutes more than half of the wall mass and contains mainly collagens and elastin, with collagen conferring rigidity to the vascular wall (23). The ratio between collagen and elastin is greater for arteries than veins, which can result in greater deformation of the portal vein compared to the artery when pressure is applied by the operator during the sonographic examination. This characteristic can explain the ellipsoid shape of the portal vein on transverse images, supported by the fact that its maximal diameter was ~37% greater than its minimal diameter, and that the diameter of the portal vein in the longitudinal view was closer to the minimal diameter obtained in the transverse view. In comparison, the maximal diameter of the aorta was only 14% greater than its minimal diameter in transverse view, with no significant difference between the diameters of the aorta in the longitudinal and transverse views. Therefore, a special effort should be made to reduce the pressure applied by the transducer on the abdomen while recording images of the portal venous system.

In human medicine, portal vein flow pulsatility is a marker of cardiogenic portal hypertension (24–26). Portal vein pulsatility index is calculated by the percentage of peak-to-peak maximum portal vein velocities; this marker is considered abnormal if the value is > 50% (26,27). Differences between minimum and maximum velocities were important in the present study. This finding may be artifactual and related to respiratory motion, as cats were not sedated. However, this difference in the maximum and minimum PV velocities was present for all cats and reflected on the pulsatility index with a median of 0.65 and a relatively small interquartile range (0.57 to 0.7). Although it could be artifactual, a species-specific finding cannot be completely excluded. A recent study performed in sedated healthy cats also reported a portal pulsatility of 0.72 (28), comparable to our study. Some reports in human medicine also describe a pulsatile portal vein flow in normal human patients (24); therefore, this marker may not be accurate and should be interpreted with caution in cats. Portal congestion index has been used in hepatic hemodynamic evaluation in veterinary medicine (29,30) and has been associated with chronic liver diseases in human medicine (31). There was a positive correlation between the congestion index and the portal venous pressure in humans, suggesting that the congestion index may be another marker for portal hypertension. Congestion index values of the portal vein have apparently not been reported in the feline population, but a study in 6 healthy dogs reported a median portal congestion index equal to 0.032 cm/s (32), comparable to the mean congestion index obtained in our study.

Our study had some limitations. First, every cat was considered healthy based on physical examination and clinical history, but no comprehensive blood work or urine analysis was done for the study. Such diagnostic tests could have identified patients with early-stage hepatobiliary disease but without clinical signs. Although hepatobiliary diseases may result in abnormal sonographic findings, some pathologic processes may appear unremarkable on ultrasound despite the presence of liver disease (4,33–35). Secondly, several cats still had food in their gastrointestinal tract at the time of the ultrasound. Although the influence of recent food ingestion on ultrasonographic characteristic of the portal vein has not been determined in the feline population, transient increases in portal vein pressure have been reported in dogs postprandially (35). Further studies are needed to assess the influence of food ingestion on the hemodynamics of the portal venous system in cats. Lastly, special effort was made to reduce the pressure applied by the transducer as it may cause distortion of the vessels and could affect the measurements obtained. It would have been relevant to look at intra- and inter-operator repeatability and reproducibility of the results obtained.

Our study provided sonographic data of the portal vein and its intra-hepatic branches in healthy, unsedated cats. Despite a relatively small sample size, this is the largest population ever described in a prospective study. Diagnosing hepatobiliary disease can be challenging and those values may be used in the diagnostic evaluation of the feline liver. Sonographic measurements outside these ranges could reflect hemodynamic abnormalities of the portal venous system in cats.