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ORIGINAL RESEARCH

Value of Complete Full-length Lower

Extremity Sonography in Patients
Undergoing Computed Tomographic
Pulmonary Angiography
Gajan Sivananthan, MD, Neil J. Halin, DO, James M. Estes, MD, Jean M. Alessi-Chinetti, RVT, RDMS,
Joseph F. Polak, MD, MPH
ObjectivesTo evaluate the diagnostic yield of complete lower extremity venous
sonography for diagnosing deep venous thrombosis (DVT) in patients undergoing
computed tomographic (CT) pulmonary angiography for suspected pulmonary
embolism (PE).
MethodsWe retrospectively reviewed all cases of lower extremity venous sonography and CT pulmonary angiography performed within 1 day of each other (n = 147)
in a tertiary care center. Indications for the studies performed, angiographic findings,
sonographic findings, age, sex, inpatient/outpatient status, lower extremity symptoms,
and treatment status were recorded. Prevalence rates and patient characteristics were
compared by 2 and Fisher exact probability tests where appropriate. Multivariable
logistic regression with acute PE as the outcome was performed for age, sex, interval
between angiography and sonography, indication for angiography, inpatient/outpatient status, and venous sonographic findings.

Received December 11, 2013, from the Departments of Radiology (G.S., N.J.H., J.F.P.) and
Vascular Surgery (J.M.E., J.M.A.-C.), Tufts Medical Center, Boston, Massachusetts USA. Revision
requested January 6, 2014. Revised manuscript
accepted for publication March 28, 2014.
Address correspondence to Gajan Sivananthan,
MD, Department of Radiology, Tufts Medical
Center, 800 Washington St, Box 299, Boston, MA
02111 USA.
E-mail: gsivananthan@tuftsmedicalcenter.org
Abbreviations

ACCP, American College of Chest Physicians;

CT, computed tomographic; DVT, deep
venous thrombosis; IVC, inferior vena cava;
PE, pulmonary embolism
doi:10.7863/ultra.33.12.2137

ResultsThe prevalence of PE (23.8%) was similar to the prevalence of DVT (27.9%).

Angiographic findings were not associated with the interval between angiography and
sonography or inpatient/outpatient status. Acute DVT was more likely (P = .0009)
when angiographic findings were positive (51.4%), but DVT prevalence was still
substantial (20.5%) in patients with negative angiographic findings. Lower extremity
symptoms were not associated with DVT in cases with negative angiographic findings
(P = .48). Eighteen of the 23 patients with acute DVT and negative angiographic findings were treated.
ConclusionsThere is a high rate of DVT in a population undergoing CT pulmonary
angiography for suspected PE even when PE is not diagnosed. Our data apply to a tertiary care institution, suggest a surveillance bias, and favor the utility of venous sonography in this population.
Key Wordscomplete venous sonography; computed tomographic pulmonary angiography; deep venous thrombosis; distal deep venous thrombosis; proximal deep venous
thrombosis; pulmonary embolism; vascular ultrasound

ulmonary embolism (PE) and deep venous thrombosis

(DVT) are strongly associated with each other. The incidence of PE in the United States is estimated to be 1 per 1000
persons per year, and the diagnostic rate has increased with the use of
spiral computed tomographic (CT) scans.1,2 Clinical scoring systems
complemented by selective imaging have led in most instances to better detection rates, early treatment, and improved outcomes.3

2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:21372143 | 0278-4297 | www.aium.org

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SivananthanLower Extremity Sonography in Patients Undergoing CT Pulmonary Angiography

Computed tomographic pulmonary angiography is

considered the reference standard for evaluation of
patients with suspected PE.4 Lower extremity venous
sonography in patients with clinical symptoms of concern
for PE has shown various diagnostic yields depending on
the use of either single-detector57 or multidetector CT
scanners.8,9 Although lower extremity sonography can be
performed in patients with positive angiographic findings
to further risk stratify patients and to guide therapy such
as placement of an inferior vena cava (IVC) filter,10 it is less
commonly performed in patients with negative angiographic findings.
Given the increasing use of clinical scoring systems1113
(Tables 1 and 2) before CT pulmonary angiography is
done, shared risk factors for DVT and PE, and the possibility that a surveillance bias might increase disease prevalence,14 it is likely that patients with negative angiographic
findings still have a high a priori probability of thromboembolic disease and a substantial prevalence of lower
extremity DVT.
The purpose of our study was to evaluate the diagnostic yield of lower extremity venous sonography for
diagnosing DVT in patients undergoing CT pulmonary
angiography and to examine associations between the
presence or absence of PE with lower extremity symptoms
and the location of DVT in the lower extremities.

Materials and Methods

We retrospectively reviewed all of the cases of lower
extremity venous sonography and CT pulmonary angiography performed in our institution, a tertiary care center,
over a 4-year period. The study was conducted after review
and approval by our Institutional Review Board.
Of the 8305 lower extremity venous sonographic
studies and the 2054 CT pulmonary angiographic studies
performed, we identified a group of 160 consecutive CT
pulmonary angiographic studies and lower extremity
venous sonographic studies performed within 1 day of
each other. We excluded 6 instances of indeterminate CT
pulmonary angiographic studies and 7 instances of CT pulmonary angiographic studies performed in patients without
symptoms of PE but with symptoms of DVT or known DVT.
We studied the associations between angiographic and
sonographic findings in 147 instances, including 4 patients
who had undergone CT pulmonary angiographic and
venous sonographic studies on 2 separate visits separated
by an interval of greater than 90 days.
We recorded demographic information, including
patient age, sex, and inpatient/outpatient status at the time
2138

of the first examination. We also reviewed the primary indication for the study and the patient information sheet provided for each study.
Computed Tomographic Pulmonary Angiography
Computed tomographic pulmonary angiography was performed on either a Somatom Sensation (16-detector) or a
Somatom Definition (64-detector) device (Siemens AG,
Forchheim, Germany). Studies were performed after injection of 70 mL of iopamidol (Isovue 370; Bracco SpA,
Milan, Italy) at a rate of 5 mL/s. Acquisition was started
from a locator slice centered on the main pulmonary artery
when the average density within a region of interest reached
40 Hounsfield units above the baseline Hounsfield unit.
Diagnosis of an acute pulmonary embolus was made
in cases of a central intraluminal filling defect, a peripheral
intraluminal filling defect forming acute angles with a vessel
wall, or total cutoff of vascular enhancement. A diagnosis
of a chronic pulmonary embolus was made in cases of
Table 1. Wells and Simplified Wells Scores
Simplified
Wells Score Wells Score

Parameter
Clinical signs and symptoms of DVT
PE most likely diagnosis
Surgery or bedridden for >4 d
within the past 4 wk
Previous PE or DVT
Heart rate >100 beats/min
Hemoptysis
Active cancer

3
3

1
1

1.5
1.5
1.5
1
1

1
1
1
1
1

Wells score: 4 or lower, low pretest probability; 4.5 to 6, moderate pretest

probability; higher than 6, high pretest probability. Simplified Wells score:
1 or lower, PE unlikely; higher than 1, PE likely.
Table 2. Revised Geneva and Simplified Revised Geneva Scores

Parameter
Age 65 y
Previous PE or DVT
Surgery or fracture within 1 mo
Active cancer
Unilateral lower extremity pain
Hemoptysis
Heart rate 7594 beats/min
Heart rate >94 beats/min
Unilateral lower extremity edema
and tenderness

Revised
Geneva Score

Simplified
Revised
Geneva Score

1
3
2
2
3
2
3
5

1
1
1
1
1
1
1
2

Revised Geneva score: 0 to 3, low pretest probability; 4 to 10, moderate

pretest probability; higher than 11, high pretest probability. Simplified
revised Geneva score: 0 to 2, PE unlikely; higher than 2: PE likely.

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SivananthanLower Extremity Sonography in Patients Undergoing CT Pulmonary Angiography

mural-based intraluminal defects forming obtuse angles with

the vessel wall. Intimal irregularities including bands and
webs were also diagnosed as chronic pulmonary emboli.
Venous Sonography
Lower extremity venous sonography was performed on
either a LOQIQ 700 or LOGIQ 9 device (GE Healthcare,
Waukesha, WI) equipped with linear array 7-9L 510-MHz
and 9L 2.58-MHz transducers. The imaging protocol
included comprehensive compression sonography of the
deep veins from the groin to the lower calf by displacing an
ultrasound transducer in the transverse plane by 1 to 2 cm.
The anterior tibial veins were not routinely interrogated.
In addition to the conduit veins, the soleal and gastrocnemius veins were compressed. A Doppler waveform (with
augmentation) was obtained for the common femoral, mid
femoral, and popliteal veins. A transverse color Doppler
image of the calf veins in the mid calf was also obtained during
an augmentation maneuver. The primary diagnostic criterion was loss of compressibility within a specific venous
segment. Color Doppler imaging was used for confirmation.
The appearance of the noncompressible segment of the
vein was further evaluated for the location of the thrombus
and its echogenicity. Areas of mural thickening with
echogenicity similar to that of the surrounding soft tissues
were considered to represent chronic wall changes. In all
such cases, the pattern of blood flow in the lumen was verified with color Doppler imaging and, when needed, with
B-flow imaging.
Statistical Analysis
The prevalence rates of PE and DVT are reported as percentages (95% confidence intervals). 2 statistics were
used to compare clinical characteristics of cases with positive and negative lower extremity venous sonographic
findings. A Fisher exact probability test was used to evaluate the significance between the presence of PE, DVT, and
lower extremity symptoms. Multivariable logistic regression with acute PE as the outcome was performed for the
following variables: age, sex, interval between the angiography and sonography, indication for angiography, inpatient/outpatient status, and venous sonographic findings.
A standard statistical package (JMP 9.0; SAS Institute Inc,
Cary, NC) was used.

Results
The mean age of the population SD was 58.7 17.4 years
with 39.2% men (56 of 143). At the time of the studies, most
patients were inpatients (73.5% [108 of 147]). There were
J Ultrasound Med 2014; 33:21372143

46 instances of PE, 11 of which were chronic, for a rate of

acute PE of 23.8% (35 of 147). The rate of acute DVT was
27.9% (41 of 147). The venous sonography was technically limited in the right leg in 3 patients (2 with DVT in
the left leg), in the left leg in 4 patients (2 with DVT in the
right leg), and in both legs in 2 patients. There were 20
instances of chronic venous changes manifested as wall
thickening. Of these, 8 were bilateral and 12 unilateral. One
patient with chronic changes had acute DVT on the contralateral side. There were 6 patients with bilateral DVT,
4 with bilateral DVT isolated to calf veins. The presence
of acute DVT was not associated with age (P = .07) or
inpatient/outpatient status (P = .55) but slightly with male
sex (P = .04). The indications for venous sonography with
respect to the study sequence and sonographic findings are
provided in Tables 3 and 4, respectively. There was no
association between a specific indication and positive
sonographic findings (P = .5). The sonographic examination was performed first in 56% of cases (82 of 147) and
correlated with the presence of lower extremity symptoms
(P = .0004). However, the sequence of studies did not correlate with the presence of acute PE or DVT.
The results of the multivariable logistic regression
analysis with acute PE as the outcome are presented in
Table 5.The median interval between venous sonography and
CT pulmonary angiography was 0.3 days. Primary indicaTable 3. Indications for Venous Sonography Versus Study Sequence
Parameter

Angiography
First (n = 65)

Bed rest
Pain
Shortness of breath
Swelling
Miscellaneousa

Sonography
First (n = 82)

5
13
31
10
6

8
33
12
21
8

aHistory of DVT, positive D-dimer results, and hypoxia.

Table 4. Indications for Venous Sonography

Indication
Bed rest
Pain
Shortness of breath
Swelling
Miscellaneousa

Negative
Sonographic
Findings
(n = 106)

Positive
Sonographic
Findings
(n = 41)

Total

8
30
32
25
11

5
16
11
6
3

13
46
43
31
14

aHistory of DVT, positive D-dimer results, and hypoxia.

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SivananthanLower Extremity Sonography in Patients Undergoing CT Pulmonary Angiography

tions for CT pulmonary angiography were shortness of

breath (n = 90 [61.2%]), hypoxia (n = 19 [13%]), chest
pain (n = 13 [8.8%]), rule out PE (n = 12 [8.2%]), tachycardia (n = 6 [4%]), and miscellaneous causes (n = 7
[4.7%]). There was a negative correlation between the
indication of shortness of breath and positive angiographic
findings compared to all other indications. There was no
correlation between positive angiographic findings and age,
sex, interval between angiography and sonography, and
inpatient/outpatient status.
The presence of acute PE was strongly associated with
the presence of acute DVT, with 18 of the 35 patients with
positive angiographic findings (51.4%; 95% confidence
interval, 37%68%) having acute DVT (P = .0009),
whereas 23 of the 112 patients with negative angiographic
findings (20.5%) had acute DVT (P = .0017). The distribution of DVT was also different between both groups. Of the
35 patients with PE, 12 (34.3%) had proximal DVT, and 6
had isolated calf vein DVT, whereas this pattern was
reversed for the cohort of 112 patients without PE, in
which 6 (5.4%) had proximal DVT, and 17 had isolated
calf vein DVT. Deep venous thrombosis in patients without PE was more likely to be isolated calf vein DVT compared to patients with PE (P = .01).
Of the 35 patients with positive angiographic findings
(Table 6), 13 had lower extremity symptoms, whereas 22
did not. Patients with lower extremity symptoms were more
likely to have DVT (proximal or isolated calf vein) than
patients without lower extremity symptoms (P = .005).
Of the 112 patients with negative angiographic findings,
66 had lower extremity symptoms (Table 7). Patients with
lower extremity symptoms were not more likely to have
DVT (proximal or isolated calf vein) than patients without symptoms (P = .48).

Follow-up was available in all of the 23 patients with

lower extremity DVT and angiographic findings for acute PE.
Fifteen patients were treated with anticoagulation, and 3
with insertion of an IVC filter. Three patients were already
receiving anticoagulation therapy for prior PE. Two patients
with isolated calf vein DVT were not treated: 1 had followup sonography for thrombus extension, and the other
already had an IVC filter in place. Fourteen of the 18 patients
treated with anticoagulation therapy or an IVC filter had
isolated calf vein DVT.

Discussion
We found that the rate of DVT in patients undergoing CT
pulmonary angiography was high, irrespective of positive or
negative angiographic findings for PE. Although the rate of
DVT in patients with PE was 51.4%, it was still substantial,
at 20.5%, in patients with negative angiographic findings.
In our practice, positive venous sonographic findings led
to anticoagulation or IVC filter placement in 18 of 23 cases
that had positive sonographic findings for DVT despite
negative angiographic findings.
Our detection rate for DVT in the proximal deep veins
in patients with negative angiographic findings was 5.4%
(95% confidence interval, 2.5%11.2%), which was higher
than the values of 2.4%, 3%, and 3.7% reported by other
investigators but within the 95% confidence intervals.1517
By performing a complete lower extremity sonographic
examination, our overall rate for DVT increased to 20.5%
Table 6. Patients With Positive CT Pulmonary Angiographic Findings

Finding
Any DVT
Proximal DVT

Table 5. Multivariable Logistic Regression With Acute PE as Outcome

Indication

OR

Age, per y
Male
Interval between studies, h
Sonography first
Indicationa
Inpatient
Positive sonographic findings

1.02
1.85
1.01
0.59
0.40
1.76
3.90

Lower
Upper
95% OR 95% OR
0.99
0.84
0.96
0.24
0.18
0.71
1.66

1.04
4.08
1.06
1.42
0.87
4.40
9.60

P
.21
.13
.74
.26
.02
.22
.0017

OR indicates odds ratio.

aIndication was collapsed as shortness of breath versus nonshortness
of breath after preliminary analyses showed only shortness of breath to
be significant as a variable.

2140

Lower Extremity
Symptoms
(n = 13)
11/13 (61.1)
8/11 (72.7)

No Lower Extremity
Symptoms
(n = 22)
P
7/22 (38.9)
4/7 (57.1)

.005
.63

Data are presented as number (percent) for differences in the presence

and location of DVT by a likelihood ratio of 0.006 given some cells with
less than 5 elements to use the Fisher exact test. Likelihood of lower
extremity pain in cases with PE (13/35 [37.1%]) compared to pain without PE (66/112 [58.9%]): P = .032 (2 sided).
Table 7. Patients With Negative CT Pulmonary Angiographic Findings

Finding
Any DVT
Proximal DVT

Lower Extremity
Symptoms
(n = 66)
12/66 (18.2)
4/12 (33.3)

No Lower Extremity
Symptoms
(n = 46)
P
11/46 (24.9)
2/11 (18.2)

.48
.64

Data are presented as number (percent).

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SivananthanLower Extremity Sonography in Patients Undergoing CT Pulmonary Angiography

because of the added detection of isolated calf vein DVT.

Few studies have included evaluation of the distal calf veins
when studying the efficacy of venous sonography in
patients with suspected PE but negative CT pulmonary
angiographic findings. Our detection rate for proximal
DVT in patients without PE was similar to that reported
by Elias et al18 (4.4%) but higher than the rate reported for
isolated calf vein DVT (11.8%).
The distinction between proximal and isolated calf
vein DVT is an important one. The natural history and risk
of proximal extension of isolated calf vein DVT are quite
variable, with studies showing the risk of proximal extension between 0% and 44%. The large variation is attributed
to the heterogeneity of the study populations and designs.19
In the Calf Deep-Vein Thrombosis in High-Risk Symptomatic Outpatients study,20 isolated calf vein DVT was present in 15% of high-risk symptomatic outpatients, but
proximal extension within 1 week only occurred in 3%,
whereas 90% had complete resolution without anticoagulation therapy. However, in that study, 1 patient with isolated calf vein DVT who did not receive anticoagulation
therapy (1.6%) died of fatal PE during a 3-month follow-up
period.20 These data suggest that 90% of patients with isolated calf vein DVT might not need to be treated with anticoagulation therapy, but these patients are hard to identify
at the time that the isolated calf vein is initially detected.
It is believed that isolated calf vein DVT does not carry the
same risk for PE as does proximal DVT, and its management continues to be controversial. The 2008 American
College of Chest Physicians (ACCP) guidelines for treatment of patients with thromboembolic disease without risk
factors for proximal extension gave a weak (2B) recommendation for therapeutic anticoagulation.21 The 2012
ACCP guidelines have become weaker (2C recommendation), in favor of 1-week follow-up lower extremity
sonography.22 However, the guidelines still recommend
treatment for patients with severe symptoms or with risk
factors for extension as well as patients who would be
inconvenienced by repeated testing.23,24 Most of our patients
with isolated calf vein DVT were treated, a pattern consistent with the 2008 ACCP guidelines.24 It is likely that the
2012 ACCP guidelines may cause a larger proportion of
our patients with positive findings for DVT to have followup sonographic examinations, but this hypothesis has yet
to be confirmed.
We have found that patients with PE and lower
extremity symptoms have a higher percentage of proximal
DVT than isolated calf vein DVT. Intuitively, this finding
makes sense and was also suggested in a study by Girard
et al.25 These data are consistent with the belief that isoJ Ultrasound Med 2014; 33:21372143

lated calf vein DVT is associated with less severe forms of

thromboembolic disease and a less intense inflammatory
response.26,27 We cannot comment on this likelihood,
since most of our cases of calf vein DVT were treated. It is
possible that without treatment, our patients would have
shown progression of DVT into the thigh or would
have had symptomatic PE. Prospective evaluation of risk
factors with short- and perhaps long-term clinical and
venous sonographic follow-up will be needed to study the
associations between risk factors and the prognosis of isolated calf vein DVT.
In our cohort, patients clinically suspected of having a
pulmonary embolus who were evaluated with both
CT pulmonary angiography and complete lower extremity compression sonography had similar prevalence rates
for DVT (27.9 %) and PE (23.8%). This high prevalence
is unlikely to be due to a bias toward individuals with lower
extremity symptoms, since, overall, 53.7% of our patients
(79 of 147) had lower extremity symptoms. In addition,
leg symptoms by themselves did not directly correlate with
the presence of DVT. The high prevalence is more likely
due to the shared pathogenesis of PE and DVT, with
similar risk factors predisposing to both PE and DVT.
The location of the DVT was similar to that reported by
Girard et al,25 where 75% of DVT in patients with PE was
proximal DVT, and 25% was isolated calf vein DVT. In our
study, 66% of cases were proximal, and 33% were distal.
The slight difference is likely due to the fact that we evaluated for soleus and gastrocnemius DVT, whereas Girard
et al25 did not. The lack of correlation with the sequence of
the studies (ie, whether angiography or sonography was
performed first), inpatient/outpatient status, and indication
for the angiography or sonography suggests that factors
not included in our analysis are at work. The negative correlation between shortness of breath and positive angiographic findings is surprising and likely reflects the low
specificity of this symptom.28 We believe that this finding
is an example of confounding by indication, since many
patients with shortness of breath did not have secondary
indications such as positive D-dimer results, tachycardia,
or other risk factors.
Our findings apply to a very select group of patients
seen in a tertiary care institution and do not condone the
liberal use of venous sonography as a primary approach to
the detection of PE. Rather, they likely indicate that once
individuals have been selected for a more aggressive diagnostic workup (ie, CT pulmonary angiography), the likelihood of seeing evidence of venous thromboembolic
disease at sites other than the pulmonary artery increases.
Our data also support the increasing positive yield of imaging
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SivananthanLower Extremity Sonography in Patients Undergoing CT Pulmonary Angiography

studies observed in tertiary care institutions.14 This phenomenon appears to be linked to increased clinical selection
of patients for both CT pulmonary angiographic and lower
extremity venous sonographic studies.14
Major limitations of our study include the retrospective design and the nature of our patient population, which
was representative of that seen in a tertiary care institution.
As such, the findings could be biased. We believe that any
bias, if present, is in favor of a patient subset with a high
clinical suspicion of thromboembolic disease. We cannot
support this hypothesis without prospective evaluations of
the clinical probability of PE and DVT based on decision
rules. However, our findings complement recent observations showing that a surveillance bias increases rather than
decreases the diagnostic yield of imaging tests for individuals with suspected DVT or PE.14 Were it not for this phenomenon, we would have expected much lower rates of
DVT and PE: likely on the order of 10% or less. However,
our prevalence rates for PE (23.8%) and lower extremity
DVT (27.9%) were higher than those generally reported15,16
and are consistent with the selection of a patient group
with a high a priori likelihood for thromboembolic disease.
This likely clinical selection bias can only be verified by
prospectively evaluating risk scores before venous
sonographic and CT pulmonary angiographic studies.
Our reliance on clinical data generated by the ordering
physicians could have possibly masked important clinical
traits that are associated with a higher rate of PE and DVT.
In conclusion, we found a high rate of DVT in a population undergoing CT pulmonary angiography for suspected PE. Although, as expected, this rate was high in
cases with PE, we also observed a high rate of DVT in individuals without PE, albeit mostly isolated calf vein DVT.
Our data suggest a possible patient selection bias toward a
patient subset with a high risk of thromboembolic disease
and demonstrate the possible utility of venous sonography
in this population. This hypothesis can only be further be
investigated by a prospective study.

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