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The value of contrast-enhanced color doppler ultrasound in the detection of vascularization of finger joints in patients with rheumatoid arthritis.

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Vol. 46, No. 3, March 2002, pp 647–653
DOI 10.1002/art.10136
© 2002, American College of Rheumatology
The Value of Contrast-Enhanced Color Doppler Ultrasound in
the Detection of Vascularization of Finger Joints in
Patients With Rheumatoid Arthritis
Andrea Klauser,1 Ferdinand Frauscher,2 Michael Schirmer,1 Ethan Halpern,2 Leo Pallwein,1
Manfred Herold,1 Gernot Helweg,1 and Dieter ZurNedden1
Objective. A prospective study was performed to
assess the usefulness of contrast-enhanced color Doppler ultrasound (CDUS) in the evaluation of intraarticular vascularization of finger joints in patients with
rheumatoid arthritis (RA).
Methods. We investigated 198 finger joints in 46
patients with RA, and 80 finger joints in 10 healthy
volunteers. Joints with varying levels of clinical activity
of inflammation were classified as being active, moderately active, or inactive. CDUS was performed with a
high-frequency multi-D linear array transducer. A
microbubble-based ultrasound (US) contrast agent
(Levovist; Schering, Berlin, Germany) was intravenously infused. Doppler findings were rated on the basis
of both unenhanced and contrast-enhanced CDUS images.
Results. Healthy joints showed no intraarticular
vascularization on either unenhanced or contrastenhanced CDUS. Unenhanced CDUS detected intraarticular vascularization in 7 (8%) of 83 inactive joints, in
31 (52%) of 60 moderately active joints, and in 32 (58%)
of 55 active joints. Contrast-enhanced CDUS detected
intraarticular vascularization in 41 (49%) of 83 joints
with inactive RA, in 59 (98%) of 60 joints with moderately active RA, and in all 55 joints with active RA.
Detection of intraarticular vascularization was improved by administration of the microbubble-based US
contrast agent (P < 0.001). Contrast-enhanced CDUS
demonstrated differences in intraarticular vascularization between joints with inactive RA and those with
active RA (P < 0.001), between joints with inactive RA
and those with moderately active RA (P < 0.001), and
between joints with moderately active RA and those with
active RA (P < 0.001).
Conclusion. The use of a microbubble-based US
contrast agent significantly improved the detection of
intraarticular vascularization in the finger joints of
patients with RA. This technique seems to be a useful
adjunct in the assessment of disease activity.
A crucial event in the pathogenesis of rheumatoid arthritis (RA) is the development of pannus (1).
Proliferation of pannus is an early event in the course of
the disease and can be seen before destruction of
cartilage and bone. Vascularization of pannus appears to
be crucial to its invasive and destructive behavior (2,3).
Radiography is currently the method used for assessing
the degree of actual joint destruction (4). Contrastenhanced magnetic resonance imaging (MRI) has also
been utilized for this purpose, but this technique is not
yet routinely available and is relatively cost-intensive and
time-consuming (5,6).
Hypervascularization of the pannus is usually
caused by inflammatory activity. Color Doppler ultrasound (CDUS) imaging allows for detection of vascularity (6–11). CDUS combines the imaging capabilities of
conventional B-mode ultrasound (US) with the bloodflow determinations of Doppler US and permits assessment of both the anatomy and the characteristics of
blood flow of the vessels at specific sites. However, this
technique is limited in the detection of slow flow and
flow in small vessels. The addition of recently developed
microbubble-based US contrast agents may improve the
detection of low-volume blood flow by increasing the
signal-to-noise ratio (12).
Andrea Klauser, MD, Michael Schirmer, MD, Leo Pallwein,
MD, Manfred Herold, MD, Gernot Helweg, MD, Dieter ZurNedden,
MD: University Hospital Innsbruck, Tyrol, Austria; 2Ferdinand Frauscher, MD, Ethan Halpern, MD, MSc: Thomas Jefferson University,
Philadelphia, Pennsylvania.
Address correspondence and reprint requests to Andrea
Klauser, MD, Department of Radiology II, Anichstrasse 35, A-6020
Innsbruck, Austria. E-mail:
Submitted for publication June 5, 2001; accepted in revised
form October 24, 2001.
The goal of this present study was to assess the
value of contrast-enhanced CDUS in the evaluation of
the extent of intraarticular vascularization of the finger
joints in patients with RA.
Patients and healthy volunteers. Over a period of 10
months (November 1999 until August 2000), we investigated
198 finger joints in 46 patients with RA (34 women, 12 men;
mean age 45.7 years, range 29–71 years). We examined 112
metacarpophalangeal (MCP) joints (77 MCP II and 35 MCP
III) and 86 proximal interphalangeal (PIP) joints (54 PIP II
and 32 PIP III). The patients were recruited from the rheumatology outpatient clinic of the University Hospital of Innsbruck. All patients had early RA (disease duration ⬍6 months)
and fulfilled the American College of Rheumatology (formerly, the American Rheumatism Association) criteria for the
diagnosis of RA (13).
The patients were examined by 2 rheumatologists (MH
and MS). The clinical activity of joint inflammation was
determined in accordance with the modified index of synovitis
activity, and levels of activity in the joints were classified as
active (swollen, warm, and tender), moderately active (swollen
and tender), and inactive (only swollen or neither swollen,
warm, nor tender) (14). Blood tests were performed to determine serologic activity, including measurement of hemoglobin
(Hgb), the erythrocyte sedimentation rate (ESR) (by the
Westergren method), C-reactive protein (CRP) (by nephelometry), and rheumatoid factor (RF) (by enzyme-linked immunosorbent assay for IgM-RF). The finger joints of the patients
were investigated by conventional radiography using the
Larsen score (15). Larsen stages of radiographic joint damage
(ranging from 0 to stage V) were determined for each MCP
and PIP joint. Furthermore, as controls, we examined 40 MCP
and 40 PIP joints (digits II and III of each hand) in 10 healthy
volunteers without any history of RA (7 women, 3 men) who
were in the same age range as the patients.
Color Doppler US. CDUS was performed after the
clinical investigation. CDUS was jointly performed and interpreted in consensus by 2 radiologists (AK and FF) who are
experienced in musculoskeletal US and who were blinded to
the findings of the clinical examination. Longitudinal and
transverse US scans of the MCP and PIP joints were obtained
from the dorsal view, with the joint in 20° of palmar flexion. We
used a gel standoff pad (Sonar Aid; Geistlich, Wolhusen,
Switzerland) in all cases. The CDUS examination was done
under a constant room temperature of 70°F. Film printouts
and videotape records were produced on each case.
We used a Sonoline Elegra unit with a VFX 13-5
multi-D linear array transducer, operating at a Doppler frequency of 9 MHz (Siemens Medical Systems—Ultrasound
Group, Issaquah, WA).
Unenhanced CDUS. CDUS examination was performed to detect intraarticular vascularization, which was
defined as color-flow signals in the intraarticular soft tissue or
in the pannus. Pannus was defined by its hypoechoic appearance. Vascularization was graded subjectively using a score
from 0 to 3 (Table 1). CDUS was performed in both the color
Table 1. Criteria for grading intraarticular vascularization with color
Doppler ultrasound (CDUS)
Grade of
CDUS finding
No intraarticular color-flow signals
1–5 intraarticular color-flow signals
6–10 intraarticular color-flow signals
11 or more intraarticular color-flow signals
Doppler frequency and the color Doppler amplitude (“power
Doppler”) modes. Standardized machine settings (transmit
power ⬍500 mW/cm2, a low-pass wall filter, and medium
persistence) were used and remained fixed throughout the
study. These settings were chosen to maximize sensitivity to
low-velocity and low-volume blood flow. The color Doppler
gain was optimized by increasing gain until noise appeared and
then reducing gain just enough to suppress the noise (usually
⬃60–70% gain). Color Doppler amplitude gain was optimized
by turning up the gain until first noise appeared in the
background (⬃75–85% gain). We applied the appropriate
color velocity scale using the musculoskeletal program of our
US unit. The window (color box) was restricted to the vascular
area studied. After visualization of color-flow signals, pulsedwave spectral Doppler imaging was performed using the lowest
filter setting (125 Hz) and the smallest scale available that
would display the Doppler waveforms as large as possible
without aliasing. A spectral Doppler tracing was obtained to
confirm that the color Doppler signals represented true arterial or venous flow.
Contrast-enhanced CDUS. Our study had Institutional
Review Board approval and all patients gave their written
informed consent prior to the intravenous administration of
the US contrast agent Levovist (Schering, Berlin, Germany).
This agent contains microbubbles smaller than 8 ␮m, which are
strong reflectors of the US beam and therefore improve the
strength of the blood-flow signal (Figure 1). The agent was
prepared in a standard manner. Fifteen milliliters was administered in a concentration of 300 mg/ml by continuous slowinfusion technique (16) at a rate of 1 ml/minute using a Secura
FD perfusor (Braun, Maria Enzersdorf, Austria). This infusion
technique was designed to provide uniform, optimal contrast
enhancement up to 20 minutes. Subsequently, color Doppler
frequency mode, color Doppler amplitude mode, and pulsedwave spectral Doppler imaging were performed with the same
technique as in the unenhanced imaging study.
The data obtained from unenhanced and contrastenhanced CDUS were compared with the extent of disease
activity as assessed on clinical examination.
Statistical analysis. The collected data were analyzed
using Stata software (version 7.0; Stata, College Station, TX).
The degree of vascularization obtained in the finger joints of
healthy volunteers was compared with that in patients with RA
using the Mann-Whitney 2-sample test. Differences between
the degree of vascularization on unenhanced and contrastenhanced CDUS among all subject groups were evaluated by
the Wilcoxon matched-pairs signed-rank test (17).
In order to compare the grade of intraarticular vascularity among healthy volunteers and the 3 subgroups of patients with RA, 6 sets of comparisons were required for
Table 2. Comparison of intraarticular vascularization detected with
unenhanced color Doppler ultrasound in the rheumatoid arthritis
(RA) subgroups
Grade of vascularization
Activity in RA joints
Inactive (n ⫽ 83)
Moderately active (n ⫽ 60)
Active (n ⫽ 55)
Figure 1. Schematic drawing of the effect of an intravascular
microbubble-based ultrasound contrast agent on color Doppler imaging. The microbubbles (large open circles) are stronger reflectors of
the ultrasound beam (long arrows) compared with the red blood cells
(small, clustered solid circles and short arrows).
unenhanced CDUS and 6 sets of comparisons were required
for contrast-enhanced CDUS (healthy versus inactive joints;
healthy versus moderately active joints; healthy versus active
joints; inactive versus moderately active joints; inactive versus
active joints; moderately active versus active joints). The
adjusted P value for these comparisons was 0.05 divided by 6,
or 0.008, based on the Bonferroni method. In order to evaluate
the effect of the US contrast agent for finger joint enhancement within the entire RA patient population, as well as for the
3 individual subgroups of patients with RA, 4 different comparisons of unenhanced and contrast-enhanced CDUS were
performed (entire population, inactive, moderately active,
active). The adjusted P value for these comparisons was 0.05
divided by 4, or 0.0125, by the Bonferroni method (17).
Clinical findings. On clinical examination of the
198 finger joints among 46 patients with RA, 55 joints
were classified as being active, 60 joints as moderately
active, and 83 joints as inactive. Serologic tests revealed
a mean Hgb level (⫾SD) of 131 gm/liter (⫾25), a mean
ESR (⫾SD) of 37 mm/hour (⫾23), and a mean CRP
level (⫾SD) of 24 mg/liter (⫾20). The RF was positive in
26 patients (57%). Forty-one patients (89%) had Larsen
grades 0 or I, and 5 patients (11%) had a Larsen grade II.
Results of CDUS. The US investigation was
technically adequate for examination of the MCP and
PIP joints in all patients and healthy subjects.
Healthy volunteers. Neither unenhanced nor
contrast-enhanced CDUS of the healthy joints (40 MCP
and 40 PIP joints) demonstrated detectable intraarticular color-flow signals. The mean (⫾SD) examination
Grade 0 Grade 1 Grade 2 Grade 3
time for each joint was 3 ⫾ 1.8 minutes for unenhanced
CDUS and 4 ⫾ 1.1 minutes for contrast-enhanced
Patients with RA. Unenhanced CDUS. The mean
(⫾SD) examination time per joint with the unenhanced
CDUS was 5 ⫾ 1.7 minutes. There was no significant
difference between the color Doppler frequency mode
and color Doppler amplitude mode in terms of detection
of intraarticular vascularization. Unenhanced CDUS
detected intraarticular vascularization in 7 of 83 inactive
joints (8%), in 31 of 60 moderately active joints (52%),
and in 32 of 55 active joints (58%) (Table 2).
Contrast-enhanced CDUS. The mean (⫾SD) examination time for the contrast-enhanced CDUS was
5 ⫾ 1.4 minutes. Uniform, subjectively optimal contrast
enhancement was achieved for examination times up to
20 minutes using our continuous slow-infusion technique. No substantial clinical side effects from administration of the US contrast agent were observed; 2
patients reported experiencing a sensation of “heat” at
the injection site, but this disappeared in ⬍1 minute.
Contrast-enhanced CDUS detected intraarticular
vascularization in 41 of 83 inactive joints (49%), in 59 of
60 moderately active joints (98%), and in all 55 active
joints (Table 3).
Compared with unenhanced CDUS, the use of
the US contrast agent significantly improved the detection of color-flow signals in all RA subgroups (P ⬍
0.001) and therefore allowed for improved visualization
of the extent of intraarticular vascularization (Figures 2
Table 3. Comparison of intraarticular vascularization detected with
contrast-enhanced color Doppler ultrasound in the rheumatoid arthritis (RA) subgroups
Grade of vascularization
Activity in RA joints
Inactive (n ⫽ 83)
Moderately active (n ⫽ 60)
Active (n ⫽ 55)
Grade 0 Grade 1 Grade 2 Grade 3
Based on the detection of increased intraarticular
vascularization by contrast-enhanced CDUS and the
associated high levels of serologic activity in 11 patients
with clinically moderately active RA (24%), the dose of
disease-modifying antirheumatic drug (DMARD) and
corticosteroids was increased.
Figure 2. Longitudinal dorsal ultrasound scan of the proximal interphalangeal joint, showing a small amount of pannus (arrows) in a
35-year-old patient with clinically inactive rheumatoid arthritis. A,
Unenhanced color Doppler ultrasound (CDUS) demonstrates no
intraarticular color-flow signals. This was defined as grade 0 vascularization. B, Enhanced CDUS demonstrates 2 color-flow signals, corresponding to a grade 1 vascularization.
and 3). Comparison of our results in Table 2 (unenhanced) and Table 3 (enhanced) shows that contrastenhanced CDUS is superior for the detection of vascularity, especially at higher levels of disease activity.
Contrast-enhanced CDUS showed statistically significant differences in the extent of intraarticular vascularization between the inactive and active joints (P ⬍
0.001), between the inactive and moderately active joints
(P ⬍ 0.001), and between the moderately active and
active joints (P ⬍ 0.001), using our subjective score of
vascularization (grades 0–3) (Table 4).
Figure 3. Longitudinal dorsal ultrasound scan of the proximal interphalangeal joint in a 27-year-old patient with clinically moderately
active rheumatoid arthritis. A, Unenhanced scan shows ⬍5 intraarticular color-flow signals (arrows), representing grade 1 vascularization.
B, Enhanced color Doppler ultrasound demonstrates significantly
increased intraarticular color-flow signals (arrows). The grade of
vascularization was classified as 3.
Table 4. Unenhanced and contrast-enhanced color Doppler ultrasound (CDUS) findings among the healthy volunteers and the rheumatoid arthritis (RA) subgroups*
Healthy volunteers (n ⫽ 40)
RA subgroup
Inactive (n ⫽ 83)
Moderately active (n ⫽ 60)
Active (n ⫽ 55)
0.08 ⫾ 0.3
0.98 ⫾ 0.9†‡
1.2 ⫾ 0.8†‡
0.6 ⫾ 0.5†
1.7 ⫾ 0.6†‡
2.7 ⫾ 0.4†§
* Values are the mean ⫾ SD grade of vascularization.
† P ⬍ 0.001 versus healthy volunteers.
‡ P ⬍ 0.001 versus inactive joints.
§ P ⬍ 0.001 versus inactive joints and versus moderately active joints.
Early diagnosis of RA and differentiation between inactive and active inflammation in the rheumatoid joint are critical issues for the clinician (18,19).
Structural radiographic studies are routinely used for
imaging in RA, although conventional radiology has
shown limited sensitivity and specificity in the investigation of soft tissues (20). MRI enables examination of soft
tissues (i.e., pannus) and bones, but this method has
limited availability and is very cost-intensive (20–23).
Recent studies of the small finger joints by use of US
with high-frequency transducers have been able to demonstrate bone erosions, cartilage damage, as well as local
effusion and intraarticular pannus (7,8,24).
Functional assessment of the extent of intraarticular vascularization seems to be important in evaluating
disease activity. Because hypervascularization correlates
with disease activity, CDUS may allow the identification
of RA patients with latent, but progressive, arthritis in
the small joints. In a previous study, Schmidt et al (10),
using unenhanced CDUS in patients with knee joint
synovitis, reported that the detection of intraarticular
flow signals did not correlate with the number of vessels.
However, the existing blood vessels were more intensively perfused during the inflammatory process. We
could not confirm these findings. Using contrastenhanced CDUS, we were able to detect more vessels in
the joints with active RA. Our findings may differ on the
basis of having the advantage of a US contrast agent,
which enables the detection of even slow blood flow and
blood flow in small vessels. Our observations support the
thesis stated by Schmidt et al (10), that contrastenhanced CDUS may increase the detection of even
minor perfusion.
Our results clearly demonstrate that contrast-
enhanced CDUS significantly improves the detection of
intraarticular vascularization. Without the use of the US
contrast agent, we detected intraarticular vascularization
in only 70 (35%) of the 198 inactive, moderately active,
and active joints. Contrast-enhanced imaging detected
flow signals in 155 (78%) of the 198 inactive, moderately
active, and active joints. Because of these CDUS findings and associated increased serologic parameters, the
dose of DMARD and corticosteroids was increased in 11
patients with clinically moderately active RA (24%).
However, these patients should be evaluated for clinical
outcome in a followup study. Therefore, at this time, we
do not have sufficient data to recommend contrastenhanced CDUS as a parameter for guiding therapeutic
Our use of the continuous slow-flow infusion
technique allowed examination times of up to 20 minutes (using 15 ml contrast), with uniform, subjectively
optimal enhancement. Prolonged, stable enhancement
with microbubbles contrast permits precise investigation
of up to 4 fingers. In comparison, contrast-enhanced
CDUS with the bolus technique is limited to ⬃3–4
minutes. Therefore, the infusion technique allows a
more cost-effective application of the US contrast agent.
In our series, no important clinical side effects from the
agent were noted. Only 2 patients complained about a
sensation of “heat” at the injection site, which disappeared in ⬍1 minute.
Hau et al (11) demonstrated that the extent of
intraarticular vascularization differed significantly between joints with inactive RA and those with moderately
active RA (P ⬍ 0.02) or those with active RA (P ⬍ 0.05).
Their results, using the same US equipment as that used
in the present study, are similar to our findings. However, they did not report statistically significant differences between moderately active and active joints. We
also failed to demonstrate a significant difference between moderately active and active joints with the use of
unenhanced CDUS. Using contrast-enhanced CDUS,
we found statistically significant differences between
moderately active and active joints (P ⬍ 0.001).
We conclude that the administration of the contrast agent results in improved detection of color-flow
signals, compared with the unenhanced technique. We
evaluated both the frequency and the amplitude (“power”) Doppler mode and did not find a significant difference between both techniques. This is consistent with
the findings of Schmidt et al (10), who stated that,
surprisingly, there was no higher sensitivity of power
Doppler US. However, theoretically, power Doppler
should be more sensitive in the detection of blood flow,
but this might also depend on the type of US unit (9).
Furthermore, contrast-enhanced studies will allow assessment of time intensity curves that may provide
additional information about enhancement kinetics.
This may also improve evaluation of disease activity.
Furthermore, US contrast agents should have some
advantages over MRI contrast imaging, since US contrast agents are less likely to leak into the synovial fluid
and will therefore more accurately reflect changes in the
intravascular compartment (25). Contrast-enhanced
CDUS will improve both the detection and followup of
disease activity in patients with RA.
In our study, the grading of vascularization was
subjective. Newman et al (9) used subjective grading of
vascularity on both pre- and posttherapy images and
reported good results using this technique. Furthermore,
a recent study by Walther et al (26) found a good
correlation between subjective grading by the US examiner and the histologic findings. These earlier studies
were performed without the use of a US contrast agent.
Further studies will be needed to validate subjective
quantification of contrast-enhanced color-flow signals in
order to further improve the assessment of disease
We note several limitations of our study. CDUS
findings were interpreted by 2 radiologists in consensus,
and therefore we do not have any data about inter- and
intraobserver variability. The cost of the US contrast
agent was ⬃$60 (United States dollars) per patient. The
cost of a high-end US unit, as was used for this study, is
⬃$150,000 (United States dollars). Therefore, the costeffectiveness of contrast-enhanced CDUS should be
compared with that of other techniques. Prospective
studies with a larger number of patients should be
performed, with comparison of radiographs, laboratory,
histologic evaluations, and clinical investigations in the
course of RA.
Based on our preliminary results, we conclude
that the use of a microbubble-based US contrast agent
significantly improves the detection of blood-flow signal
within the PIP and MCP joints. Contrast-enhanced
CDUS reveals significant differences in intraarticular
vascularization in the finger joints of RA patients in
association with the level of disease activity. Therefore,
this technique seems to be a helpful adjunct in assessment of disease activity in patients with RA.
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