545

Color Doppler Sonography of

Benign and Malignant Pulmonary
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Masses

Ang Yuan1’2 OBJECTIVE. The purpose of this study was to compare blood flow in benign and
Dun-Bing Chang2 malignant pulmonary masses by assessing the spectral waveforms obtained during
color Doppler sonography.
Chong-Jen Yu2
SUBJECTS AND METHODS. Fifty lung cancers in 46 patients and 28 benign lung
Sow-Hsong Kuo3
lesions in 28 patients were evaluated with color Doppler sonography. Spectral wave
Kwen-Tay Luh3
analysis of blood flow (specifically, the Doppler variables of pulsatility index, resistive
Pan-Chyr Yang2’4 index, peak systolic velocity, and end diastolic velocity) was used to determine the
distal impedance of vessels in malignant and benign pulmonary lesions.
RESULTS. The flow signal detection rates for lung cancers and benign pulmonary
lesions were 64% and 79%, respectively. All lung cancers with detectable flow signals
had either relatively low-impedance flows or arteriovenous shunting, unlike the
benign lesions, which usually had relatively high-impedance flows. For lung cancers,
the pulsatility index was 1.43 ± 0.31, the resistive index was 0.52 ± O.i3, peak systolic
velocity was 0.17 ± 0.07 m/sec, and end diastolic velocity was 0.07 ± 0.03 m/sec. For
benign lung lesions, the pulsatility
index was 3.32 ± 0.68, the resistive index was 0.90
± 0.06, peak systolic velocity was
0.28 ± 0.09 m/sec, and end diastolic velocity was
0.03 ± 0.01 m/sec. All four variables were significantly different (p < .001) between
lung cancers and benign lung lesions. When a cutoff value of mean ± 2 SD was used,
the resistive index and pulsatility index were shown to be sensitive and specific for
the diagnosis of lung cancer (sensitivity, specificity = 1 00%, 95% for resistive index;
97%, 95% for pulsatility index). Flow was detected less often in squamous cell carci-
noma than in adenocarcinoma and small-cell carcinoma.
CONCLUSION. We conclude that color Doppler sonography is useful for showing
vascularity in pulmonary masses, and may be helpful in differentiating malignant from
benign lung tumors.

Received December 30, 1993; accepted after

revisionApril 15, 1994. AJR 1994;163:545-549

Supported by grant NSC-83-041 2-B-002-1 37

from the National Science Council of the Republic
of China. The angiogenesis of a malignant tumor is closely linked to its growth and meta-
1 Department of Emergency Medicine, National static potential [1-10]. Recently, color Doppler sonography has been found to be
Taiwan University Hospital, Taipei 100, Taiwan, Re- useful for detecting blood flow signals in vessels of malignant tumors by means of
public of China.
continuous-wave, pulsed-wave Doppler, and color flow mapping techniques [ii-
2Department of Internal Medicine, National Tai-
20]. Doppler spectral waveforms (time-velocity waveforms) can also be used to
wan University Hospital, No. 7, Chung-Shan South
Rd., Taipei 100, Taiwan, Republic of China. Ad- assess the distal impedance of a vessel [21]. Vessels with low-impedance flow
dress correspondence to P-C. Yang. have low pulsatility and resistivity. Absence of a muscular layer in the vascular
3Department of Clinical Pathology, National Tai- wall and the presence of arteniovenous shunting in the tumor vessels usually
wan University Hospital, Taipei 100, Taiwan, Re-
cause characteristic “tumor flow signals. Thin-walled
“ vessels exhibit low-imped-
public of China.
ance signals with little systolic-diastolic variation; arteniovenous shunting anasto-
4lnstitute of Biomedical Sciences, Academia
Sinica, Taipei 100, Taiwan, Republic of China. moses show high-velocity, low-impedance flow because of a large pressure
0361 -803X/94/ 1633-0545
gradient (peak Doppler frequency shift 3 kHz) [18]. These characteristic flow sig-
© American Roentgen Ray Society nals, detected in cancers of the breast, liver, kidney, ovary, and other organs, con-
 546 YUAN ET AL. AJR:163, September 1994

relate well with histologic or angiographic findings of these Sonographic Technique

tumors [11-20]. Recent studies have also revealed that this
All patients had real-time, gray-scale sonography and color Doppler
low-impedance tumor flow is helpful in differentiating malig-
sonography with spectral wave analysis. Two sonographers performed
nant from benign tumors [10, 17, 22], and changes in blood the examination without knowledge of the clinical diagnosis. Studies
flow in malignant tumors have some value in predicting the were done with a color Doppler sonognaphic unit (Toshiba SSA-270A,
tumor’s response to chemotherapy [22]. Although sonogra- Tokyo) with a 3.5-MHz convex probe, which had a pulse repetition fre-
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phy is useful in the diagnosis of various diseases of the chest quency of up to 15 kHz. First, the mass was localized with real-time,
[23-26], flow signals in lung cancer have not been carefully gray-scale sonography, and the size (largest diameter) of the lesion
studied [27]. We designed a prospective study to assess the was measured. Then, color Doppler mapping of the entire mass was
Doppler flow characteristics of pulmonary masses to deter- done to detect blood flow. Sensitivity to low velocity (Doppler frequency
mine whether the flow patterns are different in benign and shifts) was maximized by choosing a low-velocity scale (0.26 m/sec for
a Doppler angle of O or 180#{176}),whereas the wall filter (up to 100 Hz)
malignant tumors.
was set at a level to minimize rejection of small frequency shifts (low-
velocity flow) and also to avoid interference from respiratory or cardiac
movement. Color Doppler gain was increased until background noise
Subjects and Methods
was apparent as a colored “snowstorm” across the image and was
Study Population then decreased until only a few random specks remained visible. The
From December 1991 to December 1992, inpatients who had chest mass was scanned slowly from margin to margin to detect blood flow,
radiographs that showed a pulmonary mass that was suspected to be a which usually appeared as persistent areas of color with a curvilinear,
malignant tumor were referred for color Doppler sonognaphy. The inclu- tubular, or branching distribution on real-time images. When blood flow
sion criteria were that the pulmonary lesions be accessible with was detected on color Doppler sonograms, pulsed-wave Doppler was
“ultrasonic windows” [23-26] and that the patients be cooperative and used, with the Doppler gate focused on the center of the flow signals
able to hold their breath temporarily to minimize interference from move- and the transducer adjusted so that the Doppler angle 0 between the
ment ofthe chest wall while the flow signal was being acquired. An ultra- flow signals and the ultrasound beam was 60’ or less. We used pulsed-
sonic window exists when the tumor contacts directly with the parietal wave Doppler sonography to sample all the flow signals in the tumor for
pleura, or when there is an area of consolidation between the centrally spectral wave analysis. At least three vessels were sampled, and the
located tumor and the parietal pleura so that the ultrasound beam can measurements were repeated at least three times. Spectral waveforms
penetrate to the lesion without the interference of interposing air [23-26]. that were reproducibly similar over three consecutive cardiac cycles
During this period, a total of 126 inpatients with suspected pulmonary were regarded as satisfactory. Each spectral waveform was then
tumors were seen at National Taiwan University Hospital. Forty patients recorded on a laser disk so that the Doppler indexes and Doppler angle
were not examined with color Doppler sonognaphy because of lack of an could be measured and calculated later.
accessible ultrasonic window. Twelve patients were excluded because
they had dyspnea and were unable to hold their breath temporarily.
A total of 74 patients, 44 men and 30 women 30-85 years old Quantification and Calculation
(mean age, 56 ± 1 0 years), with 78 lesions were included in this pro- The spectral waveform (time-velocity Doppler spectrum) of flow
spective study. Twenty-two of the 78 pulmonary lesions were located signal was analyzed for the following Doppler indexes: (1) pulsatility
in the right upper lobe, two were in the right middle lobe, 1 9 were in index: (peak systolic velocity end diastolic velocity)/mean
- velocity,
the right lower lobe, 17 were in the left upper lobe, and 18 were in the (2) resistive (Pourcelot) index: (peak systolic velocity - end diastolic
left lower lobe. The diameter of the lesions varied from 1 to 8 cm velocity)/peak systolic velocity, (3) peak systolic velocity (m/sec),
(average, 4 cm). Fourteen tumors were located centrally with peniph- and (4) end diastolic velocity (m/sec) [1 6, 21]. Peak systolic velocity
oral obstructive pneumonia, and 64 lesions were subpleural. and end diastolic velocity were corrected by the Doppler angle 6
The final diagnosis was confirmed by surgery in one patient, bron- between the flow signals and the Doppler gate, if the angle was not
choscopic biopsy in 20 patients, sonographically guided transthoracic 00 or 180#{176},
by using the microprocessing program in the sonographic
needle aspiration and biopsy in 30 patients, sputum cytology in 19 unit. We used the average value of each Doppler index when multi-
patients, and effusion cytology in three patients. Cultures positive for pie flow signals were detected in a tumor.
bacteria were obtained from blood in two patients, from sputum in
eight patients, and from transthoracic aspirate in seven patients. In 11
of the patients who had benign lesions, the diagnosis was based on Statistical Methods
clinical follow-ups of 3 weeks to 2 months (average, 1 month) and res-
olution offindings on serial chest radiographs after antibiotic treatment. The Kruskal-WaIIis test and Mann-Whitney rank sum test [28]
Some patients had definite diagnosis made by one or more examina- were used to compare the Doppler indexes of the spectral waveform
tions listed above. of the flow signals between malignant and benign pulmonary lesions.
Fifty malignant pulmonary tumors in 46 patients were diagnosed on A p value less than .05 was considered significant.
the basis of histologic findings (n = 12), cytologic findings (n = 36), or
both (n = 2). Twenty-eight were squamous cell carcinomas, 11 were
adenocarcinomas, and 11 were small-cell carcinomas. One patient with Results
adenocarcinoma and three patients with small-cell carcinoma had two
The prevalences of flow signals in malignant and benign
pulmonary masses each. Of 28 benign lesions, four were tuberculosis,
pulmonary masses are shown in Table 1 The pulsatility
.
one was cryptococcosis, one was organized fibrosis, one was a septic
embolus, one was a fibrous tumor, four were lung abscesses, and 16 index, resistive index, peak systolic velocity, and end dias-
were delayed-resolved pneumonia. Diagnosis of delayed-resolved tolic velocity of the flow signals in the 32 malignant tumors
pneumonia was based on one or more of the following: positive sputum and the 22 benign lesions that had detectable flow are given
culture (n = 5), blood culture positive for bacteria (n = 2), and clinical fol- in Table 2. The flow signal detection rates for lung cancers
low-up showing improvement after treatment with antibiotics (n = 11). and benign pulmonary lesions were 64% and 79%, respec-
 AJR:163, September 1994 COLOR DOPPLER SONOGRAPHY OF LUNG MASSES 547

TABLE 1 : Flow Signals in Malignant Lung Tumors and Benign the flow signals in benign lesions, which usually were high
Lung Lesions impedance and had no arteniovenous shunting (Fig. 3). All
four Doppler variables assessed were significantly different
Flow Signal Total No. of
Disease between lung cancer and benign lesions (p .001) (Table 2).
Present Masses <

Figure 4 shows the scattenplot of these Doppler indexes of

Malignant tumors flow signals in benign and malignant lesions.
Squamous cell carcinoma 13 28
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When a cutoff value of mean ± 2 SD was used, the sensi-

Adenocarcinoma 9 11
tivity and specificity of the resistive index (cutoff value, 0.78)
Small-cell carcinoma 10 11
for diagnosis of malignancy were 1 00% and 95%, respec-
Total 32 50 tively. The pulsatility index (cutoff value, 2.05) had a sensitiv-
Benign lesions ity of 95% and a specificity of 97%.
Tuberculosis 2 4 The malignant pulmonary tumors evaluated in this study
Cryptococcosis 0 1 ranged from 1 to 8 cm in diameter, including 22 smaller than
Organized fibrosis 0 1
3 cm, 21 between 3 and 6 cm, and seven larger than 6 cm.
Septic embolus 0 1
Benign pulmonary lesions ranged from 1 to 6 cm in diame-
Fibrous tumor 0 1
Lung abscess 4 4 ten, with nine smaller than 3 cm, 1 3 between 3 and 6 cm, and
Delayed-resolved pneumonia 16 16 six larger than 6 cm. The detectability of flow signals was not
dependent on the size of the masses for either the malignant
Total 22 28
or benign lesions.
Thirteen of 28 squamous cell carcinomas, nine of ii adeno-
carcinomas, and 1 0 of ii small-cell carcinomas had detectable
TABLE 2: Spectral Wave Analysis of Blood Flow Signals flow signals (Table 1). Flow was detected less often in squa-
Between Malignant and Benign Pulmonary Masses mous cell carcinomas than in adenocarcinomas and small-cell
carcinomas.
Malignant Tumor Benign Mass
Variable
(n=32) (n=22)

Pulsatility index 1 .43 ± 0.31 3.32 ± 0.68 Discussion

Resistive index 0.52 ± 0.13 0.90 ± 0.06 The lung has two arterial supplies: bronchial and pulmo-
Peak systolic velocity (m/sec) 0.17 ± 0.07 0.28 ± 0.09 nary. The spectral waveform of the bronchial circulation had
End diastolic velocity (m/sec) 0.07 ± 0.03 0.03 ± 0.01
not been described before. However, the spectral waveform
Note.-Vues are means ± SD. Differences between malignant and of the pulmonary arteries was recently evaluated with car-
benign masses were significant for all four variables (p < .001). diac Doppler sonognaphy and MR imaging [29, 30]. The
spectral waveform of the normal pulmonary artery appears
as a cone-shaped flow wave with peak velocity in the sys-
tively. The results showed that all lung cancers that had tolic phase and very low velocity (near zero) in the diastolic
detectable flow signals on color Doppler sonognams had rel- phase. The pulsatility index in the pulmonary artery is much
atively low-impedance flow (resistive index 0.77) (Fig. 1). higher than that of the low-impedance flow seen in tumors.
Five of these lung cancers had findings that suggested arte- The spectral waveforms of thin-walled vessels and artenio-
niovenous shunting, with the peak Doppler frequency shift venous shunting in lung cancers are expected to reflect low-
ranging from 3.0 to 3.8 kHz (Fig. 2). This was in contrast to impedance flow, that is, flow waves with high velocity in dias-

Fig. 1 .-Dupiex Doppler sonogram of a 6 x 3 Fig. 2.-Duplex Doppler sonogram of a 5 x 3 Fig. 3.-Duplex Doppler sonogram in 67-
cm isoechoic mass (adenocarcinoma) in lower cm hypoechoic mass (adenocarcinoma) in upper year-old man with pulmonary tuberculosis in
lobe of right lung. Spectral waveform of flow sig- lobe of left lung shows blood flow at margin of tu- lower lobe of left lung shows several blue and
nais at margin of mass shows low-impedance mor near pleura. Spectral waveform reveals arte- red flow signals in massiike lesion. Spectral
flow with small variation between systolic and di- riovenous shunting: low-impedance flow with waveform reveals high-impedance flow. Pulse-
astolic waves. Pulsatllity index and resistive in- high systolic and diastolic velocities. Pulsatility tility index = 4.20, resistive index = 0.93, peak
dcx are low for this flow. Puisatility index = 1.33, index = 0.90, resistive index = 0.51, peak systolic systolic velocity = 0.45 m/sec, end diastolic
resistive index = 0.52, peak systolic velocity = velocity = 0.47 m/sec, end diastolic velocity = velocity = 0.03 m/sec, Doppler angle = 21#{176}.
0.26 m/sec, end diastolic velocity = 0.15 m/sec, 0.23 m/sec, peak frequency shift = 3.8 kHz, Dop-
Doppler angle = O. pier angle = 26#{176}.
 548 YUAN ET AL. AJR:163, September 1994

Puisatlifty Resistive pulsatility and resistive indexes between benign and malignant
dex kdex adnexal masses. Consequently, although color Doppler sonog-
6.0 raphy shows promise as a noninvasive tool for characterizing
pulmonary masses, larger series of patients should be studied
5.0 1.0 to validate this technique in clinical practice.
The peak systolic velocity and end diastolic velocity of the
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spectral waveform are determined by the pressure gradient

4.0 is 0.8 #{149}
and the resistance of the vessel. The higher the resistance

3.0 Ti10.6 L of the vessel, the higher the peak systolic

lower the end diastolic velocity. A high-pressure
velocity and the
gradient

2.0 0.4
t might increase both the peak systolic velocity
tolic velocity. Consequently, the two derived variables
and end dias-
(pulsa-

3
tility index and resistive index) can be used to discriminate
0.2
vessels with different resistances. Unlike peak systolic veloc-
I .0
ity and end diastolic velocity, the pulsatility index and resis-
tive index are not influenced by the Doppler angle between
0.0 the flow signals and the ultrasound beam. It is not necessary
M B M B
to connect these values for the Doppler angle. These four
Fig. 4.-Scatterplot shows distribution of pulsatilityindexes and resistive Doppler indexes were thus chosen to assess the resistance
indexes of flow signals in malignant (M)and benign (B) pulmonary lesions. of the vessels in malignant and benign pulmonary lesions.
In this study, the malignant tumors, with their characteristic
low-impedance flow, had a lower pulsatility index, resistive
tolic phase. Because the structure of vessels in benign pul- index, and peak systolic velocity, and a higher end diastolic
monary lesions is supposed to be similar to that of normal velocity than did benign pulmonary lesions. According to Taylor
vessels, the spectral waveform is expected to reflect high- et al. [18], the continuous high-velocity signals with Doppler
impedance flow. frequency shifts of 3 kHz or more were considered indicative of
Doppler sonography has shown blood flow in tumors of many arteniovenous shunting. Therefore, the flow of arteniovenous
different organs. The differences in distal impedance of the yes- shunting had a low pulsatility index and low resistive index, but
sels in malignant and benign tumors may be helpful in distin- had high peak systolic velocity and end diastolic velocity.
guishing between these types of lesions, and the decrease in The ranges of pulsatility index and resistive index in benign
blood flow in a malignant tumor after chemotherapy on irradia- and malignant tumors have been reported for several organs.
tion may be useful for predicting response of a tumor to treat- In gynecologic malignant tumors, the pulsatility index ranges
ment [11-22]. In this study, characteristic low-impedance flow from 0.4 to 1 .5, and the resistive index is usually less than 0.70
and arteriovenous shunting were seen in lung cancers of differ- [1 7, 22]. However, in cutaneous melanoma, the resistive index
ent histologic types. These findings agree with previous reports ranges from 0.3 to 0.8 [32]. In our study, the pulsatility index in
that a low-impedance Doppler flow signal is associated with lung cancer was 1 .43 ± 0.31 and the resistive index was 0.52 ±
malignant tumors in other organs. Our results show that the 0.13. The small difference in the ranges of the pulsatility index
spectral waveform of benign pulmonary lesions is more like that and resistive index may be attributed to the different local
of the high-impedance flow seen in the pulmonary artery. This hemodynamic characteristics in different organ systems.
difference in the distal impedance between the neovascularized Squamous cell carcinoma tends to grow locally, whereas
tumor vessels and the supposedly normal-structured vessels in small-cell lung cancer and adenocarcinoma have a higher
benign lesions makes it possible to differentiate malignant pul- potential for systemic metastasis [33, 34]. This study showed
monary lesions from benign ones with colon and pulsed-wave that flow is detected less often in squamous cell carcinoma
Doppler sonography. When a cutoff value of mean ± 2 SD was than in small-cell carcinoma on adenocancinoma. The lower
used, these Doppler indexes were shown to be sensitive and detection rate of tumor flow signal in squamous cell carci-
specific for the diagnosis of malignant pulmonary tumors. noma, which reflects a smaller degree of angiogenesis in that
The high sensitivity and specificity ofthese Doppler variables tumor, may speculatively account for the lower potential for
imply a potential role of color Doppler sonography in determin- systemic metastasis in squamous cell carcinoma.
ing pulmonary malignancies. For an undiagnosed lesion in the Evaluation of the tumor flow signals in lung cancer, however,
chest, the low-impedance flow signal seen on color Doppler has some difficulties and limitations. The major difficulty we
sonograms suggests high probability of a malignanttumor. Fur- faced was the interference of respiratory movement with the
then invasive diagnostic procedures such as bronchoscopy with flow signals. If the tumor is near the mediastinum, interference
biopsy, tnansthonacic biopsy, on thoracotomy should be done from cardiac motion is unavoidable. Adjustment of the filter set-
aggressively to prove the diagnosis. On the other hand, in a ting, color gain, and sensitivity is necessary to minimize these
pulmonary lesion with high-impedance flow signals, the proba- interfering signals. In this series, flow signals from the malig-
bility of malignancy is low. To avoid excessive morbidity, an nant tumors and benign lesions were successfully assessed
invasive diagnostic procedure, such as a biopsy, might not be with color Doppler sonography, although temporary breath-
immediately necessary for these patients. In contrast to our holding was necessary in some cases. Color Doppler sonogra-
results, Hamper et al. [31] recently reported some overlap in phy cannot show blood flow in centrally located lung cancers,
 AJR:163, September 1994 COLOR DOPPLER SONOGRAPHY OF LUNG MASSES 549

which have no accessible acoustic window for the ultrasound 15. Taylor KJW, Ramos I, Morse 55, Fortune KL, Hammers L, Taylor CR.
Focal liver masses: differential diagnosis with pulsed Doppler US. Radio/-
beam to penetrate. Fortunately, centrally located lung cancers
ogy 1987;164:643-647
have a high nate of diagnosis by sputum cytology. On the other 16. Ramos IM, Taylor KJW, Kier R, Bums PN, Snower DP, Carter D. Tumor
hand, for peripheral tumors, sputum cytology has a lower diag- vascular signals in renal masses: detection with Doppler US. Radiology
nostic yield. Invasive diagnostic procedures usually are neces- 1988;168:633-637
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vascularity with transvaginal color Doppler sonography. J Ultrasound Med
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additional information about the nature of these lesions before

1991:10:563-568
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