Radiol med
DOI 10.1007/s11547-017-0730-1
ABDOMINAL RADIOLOGY
Value of blood flow velocity on color Doppler ultrasonography
for optimization of delay in scanning time on computed
tomography venography in patients with Budd–Chiari syndrome
and inferior vena cava obstruction
Peng‑li Zhou1 · Lei Yan1 · Gang Wu1 · Xin‑Wei Han1,2 · Wen‑Guang Zhang1
Received: 22 August 2016 / Accepted: 23 January 2017
© Italian Society of Medical Radiology 2017
Abstract  of the delay in scanning time during CT venography to
Purpose To prospectively determine the value of blood
flow velocity in the inferior vena cava (IVC) on color Dop-
pler ultrasonography for the optimization of the delay in
scanning time after contrast injection during computed
tomography (CT) venography in patients with Budd–Chiari
syndrome (BCS) with IVC obstruction.
Methods We enrolled 122 consecutive BCS patients with
IVC obstruction. All patients underwent color Doppler
ultrasonography, CT venography, and digital subtraction
angiography (DSA) in that order prior to treatment. The
delay in scanning time during CT venography was set at
120, 180, 240, and 300 s after contrast injection. The cor-
relation between delay in CT scanning and IVC blood flow
velocity on color Doppler ultrasonography was explored.
Image quality was classified as good, moderate, or poor.
Patients with good CT image quality were considered to
have an optimal delay in scanning time.
Results  Delays in scanning time of 120, 180, 240, and 300 s
yielded good-quality images in 2, 7, 49, and 64 patients,
respectively. The corresponding IVC blood flow velocities in
these patients were 16.10 ± 0.42 cm/s (range 15.8–16.4 cm/s),
12.90  ± 1.58 cm/s (range, 11–15 cm/s), 7.53 ± 1.35 cm/s
(range 5–10 cm/s), and 1.95 ± 1.75 cm/s (range 0–5.5 cm/s).
Conclusion  IVC blood flow velocity on color Doppler ultra-
sonography could serve as a useful tool for the optimization
L. Yan is the co-first auhtor.
* Xin‑Wei Han
hanxinwei2006@163.com
1
Department of Interventional Radiology, The First Affiliated
Hospital, Zhengzhou University, Zhengzhou, Henan, China
2
No.1, East Jian She Road, Zhengzhou 450052, Henan, China
 
ensure good-quality images for the diagnosis of BCS with
IVC obstruction.
Keywords  Budd–Chiari syndrome · Inferior vena cava
(IVC) · Computed tomography (CT) · Color Doppler
ultrasonography · Velocity
Introduction
Budd–Chiari syndrome (BCS) is a clinical disorder arising
as a consequence of the obstruction of the hepatic venous
outflow [1–3]. In Asia, membranous obstruction of the infe-
rior vena cava (IVC) and/or hepatic veins (HVs) is the most
common cause of BCS and accounts for up to 60–70% of
all BCS patients [4, 5]. Endovascular intervention with bal-
loon and/or stent is becoming the first choice of treatment
for BCS patients with membranous obstruction of the IVC
and/or HVs in China and Asia [6–10]. Prior to treatment,
the type and extent of the obstructive lesion and the status
of the circumambient structures must be clearly displayed
using color Doppler ultrasonography, computed tomogra-
phy (CT), or magnetic resonance imaging (MRI).
Currently, CT is the most widely used noninvasive diag-
nostic tool for the detection of BCS [11–15]. CT is an
excellent modality to provide information about the liver
parenchyma, cause of BCS, status of the HVs and the sple-
noportal axis, complications of chronic BCS, length of IVC
narrowing, and extra- and intrahepatic collaterals [14, 15].
However, it remains unreliable for the depiction of the IVC
outline, the circumambient structures, and the exact length
and degree of stenosis due to the use of an inappropriate
interval between contrast injection and the beginning of
scanning during CT venography.
13

BCS with IVC obstruction is a rare form of hepatic venous
outflow obstruction at the suprahepatic IVC. Due to the
obstruction, the blood flow in the proximal IVC is slow, tur-
bulent, or reversed. Thus, the blood flow velocity in the IVC
differs from person to person. To obtain clear images of the
IVC on CT venography, the technique must be optimized such
that the interval between contrast injection and the beginning
of scanning is appropriate for the blood flow velocity in the
IVC for a given patient. However, optimization of the delay
in scanning time after contrast injection according to the
blood flow velocity in the IVC, as determined on color Dop-
pler ultrasonography, has been rarely reported in the literature.
Hence, the purpose of the study was to determine the value of
IVC blood flow velocity measured using color Doppler ultra-
sonography for the optimization of the delay in scanning time
during CT venography in BCS patients with IVC obstruction.
Materials and methods
Study design
The institutional review board of our hospital approved
the study protocol, and all patients or their family mem-
bers provided informed consent before participation in the
study. From July 2012 to December 2015, 122 consecu-
tive BCS patients with IVC obstruction were prospectively
enrolled in our study. All patients underwent color Doppler
ultrasonography followed by CT venography before endo-
vascular treatment. In addition, digital subtraction angiog-
raphy (DSA) was performed after CT venography was used
to confirm the diagnosis of BCS. Patients with severe liver
failure or terminal hepatic carcinoma were excluded from
the study. Patients were divided into two groups accord-
ing to the DSA findings: partial IVC obstruction group and
complete IVC obstruction group.
Color Doppler ultrasonography
Prior to CT venography, the blood flow velocity in the IVC
was measured in all patients using color Doppler ultra-
sonography (Vivid 7 Pro, GE, USA). Blood flow velocity
was measured in the post-hepatic IVC segment avoiding
both the orifices of the HVs and collateral branches. The
blood flow velocity index was quantified as the average
peak velocity. If the blood flow in the IVC was reversed,
the velocity was recorded as zero.
CT venography
All CT venography examinations were performed on a
64-row CT scanner (LightSpeed VCT or Discovery CT750
HD, GE Healthcare). The smart preset scan technique
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Radiol med
was used for enhanced CT venography with the following
parameters: 0.625 mm × 64 slice, 120 kVp, 100–600 mA,
and 1.375:1 helical pitch. For enhanced CT venography, a
standard dose of 0.7 ml/kg body weight of contrast mate-
rial in 40 ml normal saline was administered using a power
injector at a rate of 4 ml/s through a 22-gage needle into
the antecubital vein. When the concentration of the con-
trast medium in the ascending aorta reached 100 HU, the
CT device automatically scanned an area spanning the
lower third of the heart to the inferior margin of the kid-
ney. CT images were obtained during the hepatic arterial
phase (25 s after administering the nonionic contrast mate-
rial), portal venous phase (60 s), and delayed phase (120,
180, 240, and 300 s). The acquired image data sets were
then transferred to a workstation (GE AW4.3, GE Medical),
where three-dimensional (3D) image reconstruction was
performed with a 732 × 732 matrix. The reconstruction
included the development of oblique, coronal, and sagittal
maximum-intensity projections (MIPs), multiplanar recon-
struction (MPR), and 3D volume-rendered (VR) images of
the thoracic and abdominal vascular structures.
DSA
DSA was performed by an interventional radiologist fol-
lowing the CT examinations. The access routes for angiog-
raphy were the trans-femoral approach and/or trans-jugular
approach. IVC angiography was performed using a 5-Fr
straight catheter with multiple side holes (Cook, Bloom-
ington, USA) to characterize the morphology of the IVC
and the extent of the obstruction. Two observers, who were
blinded to all clinical and previous imaging results, identi-
fied and analyzed all the DSA data together.
Image review
After reconstruction, MIP and VR images were interac-
tively evaluated by two senior radiologists working inde-
pendently. Both raters were unaware of the clinical out-
comes of the patients, and the DSA and color Doppler
results. They independently analyzed all CT venography
datasets on an offline workstation from multiple on-screen
viewing angles. The source images and the MIP, MPR,
and VR images were presented on screen, thus allowing
for adjustment of the appropriate threshold of the window
width and level. In the presence of rater disagreement in
the detection of BCS with IVC obstruction, a consensus or
majority decision was obtained.
Quantitative analysis
Image quality was evaluated on a per-patient basis and clas-
sified as good (diagnostic quality with vascular structures
Radiol med

Table 1  Baseline characteristics of the 122 BCS patients included in the study

Characteristic All patients Patients with partial Patients with complete P value
(n = 122) IVC obstruction IVC obstruction
(n = 53) (n = 69)

Age (years) 42.09 ± 10.80 43.57 ± 9.04 40.96 ± 11.92 0.187

(range 12–74) (range 28–63) (range 12–72)
Female/Male (no.) 45/77 20/33 26/43 0.995
Interval between clinical symptoms 79.28 ± 101.04 (0.25–480) 74.54 ± 93.99 (0.25–360) 82.92 ± 106.67 (0.25–480) 0.652
and treatment (month)
Length of obstruction (mm) 13.78 ± 14.70 (0.5–56) 16.53 ± 15.53 (0.5–50) 10.20 ± 12.82 (0.8–56) 0.018
Presence of thrombosis (no.) 8 (6.6) 1 (1.9) 7 (10.1) 0.050
IVC blood flow velocity (cm/s) 5.05 ± 3.95 (0-16.4) 8.18 ± 3.10 (1-16.4) 2.65 ± 2.63 (0-9) <0.001
Symptoms at diagnosis, no. (%)
 Abdominal distention 36 (29.5) 20 (37.7) 16 (23.2) 0.081
 Abdominal pain 9 (7.4) 4 (7.5) 5 (7.2) 0.950
 Varices in abdominal wall 60 (49.2) 25 (47.2) 35 (50.7) 0.697
 Ascites 35 (28.7) 18 (34.0) 17 (24.6) 0.259
 Jaundice 10 (8.2) 4 (7.5) 6 (8.7) 0.819
 Hepatic encephalopathy 2 (1.6) 1 (1.9) 1 (1.4) 0.850
 Hepatomegaly 45 (36.9) 19 (35.8) 26 (37.7) 0.835
 Splenomegaly 91 (74.6) 40 (75.5) 51 (73.9) 0.845
 GI bleeding 10 (8.2) 3 (5.7) 7 (10.1) 0.371
 Lower limb edema 49 (40.2) 23 (43.4) 26 (37.7) 0.523
 Varices in lower limbs 28 (23.0) 10 (18.7) 18 (26.1) 0.347
 Pigmentation of lower limbs 43 (35.2) 16 (30.2) 27 (39.1) 0.305
 Ulcer in lower limbs 10 (8.2) 5 (9.4) 5 (7.2) 0.662
 Child–Pugh score 6.45 ± 1.36 (5–11) 6.57 ± 1.40 (5–11) 6.35 ± 1.32 (5–11) 0.393

Values shown are expressed as mean ± standard deviation and ranges, unless otherwise indicated
BCS Budd–Chiari syndrome, IVC inferior vena cava, GI gastrointestinal

clearly visualized on MIP, MPR, and VR images), moder-
ate (vascular structures mildly limited on 3D reconstruction
due to contrast bolus or motion, but diagnostic quality with
moderate confidence), or poor (vascular structures poorly
visualized, diagnostic quality with low confidence).
κ  = 0.21–0.40; moderate, κ  = 0.41–0.60; substantial,
κ  = 0.61–0.80; and almost perfect, κ  = 0.81–1.00.
Kappa statistics with 95% confidence intervals (CIs)
were used to assess agreement between the angio-
graphic results.

Statistical analysis

All data are presented as means ± standard deviations. Results

Dichotomous and categorical data were reported as num-
bers and percentages. The χ2 test was used for categorical
variables, and the unpaired t test was used for continuous
variables. Statistical analyses were performed using SPSS
statistical software (version 13.0 for Windows, SPSS, Chi-
cago, IL, USA). P < 0.05 was considered to indicate a sig-
nificant difference.
The kappa statistic was used for comparison of
observer performance in the assessment of image
quality, IVC outline, and the upper and lower mor-
phology of the IVC obstruction. Interobserver agree-
ment was classified as follows: slight, κ  ≤ 0.2; fair,
Patient population
From July 2012 to December 2015, a total of 122 patients
were enrolled in our study. They included 77 male
patients with a mean age of 42.78 ± 11.87 years (range
12–72 years) and 45 female patients with a mean age of
40.96  ± 8.75 years (range 14–63 years). The baseline
characteristics of the patients are summarized in Table 1.
There were no significant differences in clinical signs and
symptoms between patients with partial and complete
IVC obstruction.

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 Radiol med

Fig. 1  Budd–Chiari syndrome
(BCS) with complete inferior
vena cava (IVC) obstruction in
a 55-year-old man. a A color
Doppler sonogram prior to treat-
ment shows complete obstruc-
tion of the IVC with a blood
flow velocity of 1.5 cm/s in the
post-hepatic IVC. Note also an
irregular filling defect in the
IVC (arrow). b Coronal muli-
planar reconstruction with good
image quality was obtained
using an optimal delay in scan-
ning time of 300 s; the image
shows complete obstruction
of the IVC and a thrombus in
the IVC (arrow). c An inferior
vena cavogram via the trans-
femoral approach demonstrates
complete obstruction of the
IVC and the thrombus (arrow).
The lower morphology of the
IVC obstruction on digital
subtraction angiography (DSA)
corresponded almost exactly
with the morphology depicted
on computed tomography (CT)
venography. d An inferior vena
cavogram after rupture of the
membrane shows that the extent
of the IVC obstruction on DSA
corresponds almost exactly with
that depicted on CT venography

DSA patients, 5–10 cm/s in 39 patients, 11–15 cm/s in 6 patients,

According to the reference standard, a partial IVC obstruc-
tion was observed in 53 BCS patients and a complete
IVC obstruction was observed in 69 patients. The mean
length of the IVC obstruction in all 122 patients was
13.78 ± 14.70 mm (range 0.5–60 mm). The length of the
obstruction was significantly smaller in patients with par-
tial IVC obstruction than in patients with complete IVC
obstruction (P < 0.05, Table 1).
Color Doppler ultrasonography
The mean blood flow velocity in the IVC on color Doppler
ultrasonography was 5.05 ± 3.95 cm/s (95% CI 4.35–5.76;
range 0–16.4 cm/s). The IVC blood flow velocity was sig-
nificantly greater in patients with partial obstruction than in
patients with complete obstruction (P < 0.05, Table 1).
The IVC blood flow velocity was < 5 cm/s in 61
patients, 5–10 cm/s in 49 patients, 11–15 cm/s in 9 patients,
and > 15 cm/s in 3 patients. The IVC blood flow velocity
in patients with partial IVC obstruction was < 5 cm/s in 5
and > 15 cm/s in 3 patients. The IVC blood flow velocity in
patients with complete IVC obstruction was < 5 cm/s in 56
patients, 5–10 cm/s in 10 patients, 11–15 cm/s in 3 patients,
and > 15 cm/s in 0 patients.
CT venography and color Doppler ultrasonography
Patients with good image quality on CT venography were
considered to have an optimal delay in scanning time for
an accurate diagnosis of BCS with IVC obstruction. Delay
times of 120, 180, 240, and 300 s after contrast injection
yielded good-quality images in 2, 7, 49, and 64 patients,
respectively. The corresponding mean IVC blood flow
velocities in these patients were 16.10 ± 0.42 cm/s (range
15.8–16.4 cm/s), 12.90 ± 1.58 cm/s (range 11–15.3 cm/s),
7.53 ± 1.35 cm/s (range 5–10 cm/s), and 1.95 ± 1.75 cm/s
(range 0–5.5 cm/s; Fig. 1).
Delay times of 120, 180, 240, and 300 s after contrast
injection yielded good-quality images in 2, 7, 37, and 7
patients with partial IVC obstruction, respectively. The
corresponding mean IVC blood flow velocities in these

13
Radiol med
patients were 16.10 ± 0.42 cm/s (range 15.8–16.4 cm/s),
12.90 ± 1.58 cm/s (range 11–15.3 cm/s), 7.65 ± 1.27 cm/s
(range 5.4–10 cm/s), and 4.0 ± 1.43 cm/s (range
1–5.4 cm/s). Delay times of 120, 180, 240, and 300 s after
contrast injection yielded good-quality images in 0, 0, 12,
and 57 patients with complete IVC obstruction, respec-
tively. The corresponding mean IVC blood flow velocities
in these patients were 0, 0 cm/s, 7.18 ± 1.57 cm/s (range
5–9 cm/s), and 1.70 ± 1.62 cm/s (range 0–5.0 cm/s).
The kappa value for the assessment of CT image quality
for the detection of IVC obstruction was 0.91, suggesting
excellent interobserver agreement. The kappa value for the
assessment of CT image quality for the detection of partial
IVC obstruction and complete IVC obstruction was 0.89
and 0.92, respectively.
CT venography and DSA
CT venography had a good correlation with DSA for the
diagnosis of BCS with IVC obstruction, with an accuracy
of 100%. The extent and morphology of the IVC obstruc-
tion on CT venography corresponded almost exactly with
those on DSA.
Discussion
This prospective study was designed to test the hypothesis
that good image quality on CT venography can be obtained
by optimization of the delay in scanning time according to
the IVC blood flow velocity on color Doppler ultrasonog-
raphy. Although the optimal delay in scanning time for
good image quality on CT venography did not correspond
exactly with the IVC blood flow velocity on color Doppler
ultrasonography, good image quality could be obtained
in the majority of the BCS patients with IVC obstruction
using multiple CT venography scans. Moreover, the exten-
sion and morphology of IVC obstruction on 64-row CT
venography images corresponded almost exactly with the
angiographically depicted extension and morphology of
IVC obstruction.
BCS is not an uncommon cause of hepatic venous out-
flow obstruction leading to liver disease in the Far East,
the Middle East, India, and Africa [16]. IVC obstruction,
with or without the involvement of the HVs, is the cause
of BCS in the majority of cases in these geographical areas
[17]. In BCS patients with IVC obstruction, the blood flow
velocity in the IVC varies according to the degree of steno-
sis. In patients with partial IVC obstruction, the blood flow
may be relatively fast, while in patients with complete IVC
obstruction, the blood flow may be very slow or reversed.
Hence, it is difficult to select an optimal delay in scanning
time for obtaining good-quality CT venography images.
Usually, CT venography images are obtained at 180 s
after administering the contrast medium. An inappropriate
delay in scanning during CT venography may result in the
following pitfalls: (1) The contrast medium may flow along
the IVC wall, resulting in laminar flow due to stasis of the
blood flow, and this phenomenon might be erroneously
identified as IVC thrombolysis. (2) The enhancement of the
IVC may be insufficient due to the lack of an optimal delay
in scanning, resulting in poor quality of 3D reconstructed
images. (3) Multiple scans will be required to obtain good
image quality, which increases the exposure of the patient
to radiation.
To date, few studies have evaluated the clinical implica-
tions of IVC blood flow velocity on the optimization of the
delay in CT scanning time to obtain good-quality images
for the diagnosis of BCS. In this study, we explored the
optimal delay in scanning time on CT venography accord-
ing to the IVC blood flow on color Doppler ultrasonogra-
phy. The results showed that the optimal delay in scanning
time was 120 s in patients with an IVC blood flow velocity
of > 15 cm/s; 180 s in patients an IVC blood flow velocity
of 10–15 cm/s; 240 s in patients with an IVC blood flow
velocity of 5–10 cm/s; and 300 s in patients with an IVC
blood flow velocity of ≤ 5 cm/s.
It should be noted that not all patients with an IVC
blood flow velocity of > 15 cm/s had an optimal delay in
scanning time of 120 s; in one patient, the optimal delay
was 180 s. Such exceptions also occurred in patients with
IVC blood flow velocities of 10–15, 5–10, and ≤ 5 cm/s.
Owing to differences in the examination method, manner,
and time, the status of the IVC blood flow velocity may
vary, so the above exceptions are understandable. Because
the scanning time of CT venography is very short, the
optimal delay in scanning time for obtaining good-quality
images may not be exactly 120, 180, 240, or 300 s, but
may be some time within the 120–180, 180–240, or 240–
300 s intervals. In this situation, the quality of the images
obtained may be between good and moderate. In this
study, there were only 7 patients (6.3%) in this situation;
however, the CT results correlated with the DSA findings
in all patients.
This study had some limitations. First, this was a single-
center study, and no control group was included. Second,
the number of patients was relatively small; a larger sam-
ple size is required to reach definitive conclusions. Third, to
ensure that we obtained good-quality images, we used four
different scan times for CT venography, and this may have
exposed the patients to a greater amount of radiation.
In conclusion, our findings suggest that the IVC blood
flow velocity on color Doppler ultrasonography could serve
as a useful tool for the optimization of the delay in scanning
time during CT venography to obtain good-quality images
for the accurate diagnosis of BCS with IVC obstruction.
13

Compliance with ethical standards  6. Furui Sl, Sawada S, Irie T et al (1990) Hepatic inferior vena cava
Conflict of interest statement  Peng-li Zhou declares that he has no
conflict of interest.
Gang Wu declares that he has no conflict of interest.
Xin-wei Han declares that he has no conflict of interest.
Lei Yan declares that he has no conflict of interest.
Wen-Guang Zhang declares that he has no conflict of interest.
Ethical approval All procedures performed in studies involving
human participants were in accordance with the ethical standards of
the institutional and/or national research committee and with the 1964
Helsinki declaration and its later amendments or comparable ethical
standards.
Informed consent  Informed consent was obtained from all individual
participants included in the study.
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