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Color Doppler US Pulmonary Artery Vessel Signal: A Sign for Predicting the Benign Lesions
Ultrasound in Med. & Biol., Vol. 33, No. 3, pp. 379 –388, 2007 Copyright © 2007 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/07/$–see front matter
doi:10.1016/j.ultrasmedbio.2006.08.011
● Original Contribution COLOR DOPPLER US PULMONARY ARTERY VESSEL SIGNAL: A SIGN FOR PREDICTING THE BENIGN LESIONS WU-HUEI HSU,* YANG-HAO YU,* CHIH-YEN TU,* JEN-YUAN HSU† CHIH-YI CHEN,‡ CHUN-LIEH CHEN,§ and PO-CHEUNG KWAN㛳 *Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan; Divisions of †Pulmonary and Critical Care Medicine and ‡Thoracic Surgery, Departments of †Internal Medicine, ‡Surgery, and 㛳Pathology, Taichung Veterans General Hospital, Taichung, Taiwan; and §Division of Thoracic Surgery, Department of Surgery, Feng-Yuan Hospital, Department of Health, Executive Yuan, Taiwan. (Received 12 April 2006, revised 8 August 2006, in final form 17 August 2006)
Abstract—The lung cancer blood supply originates from the bronchial artery. If vessel signals within pulmonary lesions can be confirmed to be those of the pulmonary artery, color Doppler ultrasound (US) should be able to predict and differentiate benign lesions from lung cancers. Two hundred sixty-four patients with abutting thoracic lesions (including 125 lung cancers and 139 benign lesions) underwent color Doppler US examinations. A pulsatile flow, with the vessel signal length on sonographic appearance >1 cm demonstrated by color Doppler US, was arbitrarily defined as a pulmonary artery vessel signal. Of the 264 thoracic lesions, 73 (58%) lung cancers and 107 (77%) benign lesions had detectable color Doppler US pulsatile flow vessel signals. Analyzing the pulsatile flow vessel signals, the color Doppler US pulmonary artery vessel signal was present in 74 (53%) benign lesions, but was found in only two (2%) lung cancers of a specific alveolar cell carcinoma with lobar consolidation. Using the pulmonary artery vessel signal, color Doppler US can be valuable in predicting and differentiating benign lesions from lung cancers (p < 0.0001, sensitivity ⴝ 0.53, specificity ⴝ 0.98 and positive likelihood ratio 26.5). In conclusion, color Doppler US pulmonary artery vessel signal sign is useful in predicting and differentiating benign lesions from lung cancers. (E-mail: [email protected]) © 2007 World Federation for Ultrasound in Medicine & Biology. Key Words: Ultrasonography, Doppler, Lung, Vessel, Neoplasm.
mimicking lung cancers, some semi-invasive or invasive procedures, such as thoracoscopic biopsy or surgical resection, are sometimes necessary to make a confirmative diagnosis and to exclude the possibility of lung cancers. Lung cancers are always supplied by the bronchial artery system. Thus, previously pulmonary and bronchial angiograms were used to diagnose and differentiate lung cancers from benign lesions (Lyons and Vertova 1958; Ney et al. 1972; Viamonte 1965). Among the imaging modalities used in chest medicine, color Doppler ultrasound (US) has been applied to assess the vessel signals in thoracic lesions (Gorg et al. 2003; Gorguner et al. 2003; Hsu et al. 1998, 1996; Yuan et al. 2000). Thus, from our viewpoint and experience, color Doppler US, being able to assess the vessel signals of thoracic lesions, should be able to predict and differentiate benign lesions from lung cancers.
INTRODUCTION Image [fluoroscopy, computed tomography (CT), ultrasound (US)]-guided percutaneous transthoracic needle biopsy is a well-documented technique for diagnosing thoracic tumors (Ikezoe et al. 1990; Yang et al. 1992). For malignant tumors or lung cancers, the diagnostic yields of image-guided percutaneous transthoracic needle biopsy are all ⱖ90% in published papers (Ikezoe et al. 1990; Yang et al. 1992). Nevertheless, some pulmonary benign lesions are difficult to diagnose accurately by image examinations alone and/or by image-guided percutaneous needle biopsy. Clinically, it is very important to determine the nature of thoracic lesions to make an appropriate therapeutic decision. Therefore, in the case of benign pulmonary lesions, especially lesions Address correspondence to: Dr. Wu-Huei Hsu, MD, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan. E-mail: [email protected] 379
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Herein, we describe our findings regarding the clinical application of the color Doppler US pulmonary artery vessel signal. Color Doppler US pulmonary artery vessel signal is defined as a pulsatile flow, with the vessel signal length on sonographic appearance ⱖ1 cm demonstrated smoothly by color Doppler US. Using this pulmonary artery vessel signal, color Doppler US can easily and quickly predict and differentiate pulmonary benign lesions from lung cancers with high specificity and without any risk. MATERIALS AND METHODS Patients From April 1994 to November 2001, 264 patients with thoracic lesions abutting chest wall, confirmed diagnoses and compatible clinical conditions during follow-up undergoing color Doppler US examinations were enrolled in our series. The examined patients included 207 men and 57 women, ranging in age from 17 to 88 y (mean ⫽ 58). The final diagnoses consisted of lung cancers in 125 patients and benign lesions in 139 patients. The sizes of the lung cancers, by calculating the diameter from chest radiographs, ranged from 2.0 to 13.0 cm, with a mean of 6.5 ⫾ 2.4 cm; and the sizes of the benign lesions ranged from 1.7 to 12.0 cm, with a mean of 6.9 ⫾ 2.5 cm. The proven cytologic and/or histologic diagnoses of the 125 lung cancers were squamous cell carcinoma (n ⫽ 62), adenocarcinoma (n ⫽ 38), small cell carcinoma (n ⫽ 14), adenosquamous carcinoma (n ⫽ 4), large cell carcinoma (n ⫽ 2) and poorly differentiated carcinoma (n ⫽ 5, non-small cell lung cancer type). The diagnoses of lung cancers were made by the following methods: US-guided needle biopsy (n ⫽ 98), transbronchial biopsy (n ⫽ 21), lymph node aspiration or surgical biopsy (n ⫽ 6), surgical resection (n ⫽ 38, including craniotomy in one) and sputum cytology (n ⫽ 6). Of these, 38 patients had a positive cytologic and/or histologic diagnosis made by two or more of the examinations listed above. Among the 125 patients with proven lung cancers, four were initially diagnosed as squamous cell carcinoma (n ⫽ 3) and adenocarcinoma (n ⫽ 1) by US-guided fine needle aspiration biopsy; however, a final diagnosis of adenosquamous carcinoma was confirmed by surgical resection. Another two were also misdiagnosed as poorly differentiated squamous cell carcinoma by US-guided fine needle aspiration biopsy, but adenocarcinoma was proven by US-guided large-bore cutting biopsy (n ⫽ 1) and surgical resection (n ⫽ 1). The diagnoses of the 139 benign lesions were made by the following methods: surgical resection in 16 [tuberculoma (n ⫽ 4), cryptococcosis (n ⫽ 2), organized
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pneumonia (n ⫽ 3), pulmonary sequestration (n ⫽ 4), mucormycosis (n ⫽ 1), actinomycosis (n ⫽ 1) and congenital cystic adenomatoid malformation (n ⫽ 1)]; USguided fine needle aspiration with positive causative microorganisms in 17 [lung abscess (n ⫽ 8), cryptococcosis (n ⫽ 6), actinomycosis (n ⫽ 2) and tuberculous granulomatous inflammation (n ⫽ 1)]; US-guided fine needle aspiration and surgical resection in two (cryptococcosis, progressive change in the lung lesions in spite of medical managements), positive causative microorganisms in two [lung abscesses, by transbronchial brush (n ⫽ 1) and blood culture (n ⫽ 1)]; exudative tuberculous pneumonia with confirmed diagnoses and compatible clinical conditions during follow-up in 12 [positive sputum acid-fast stain and culture (n ⫽ 5), positive sputum culture (n ⫽ 6) and pleural biopsy (n ⫽ 1)]; tuberculous granulomatous inflammation with compatible clinical condition in two [positive sputum acid-fast stain (n ⫽ 1) and sputum culture (n ⫽ 1)]; nocardiosis with positive sputum gram stain in three and compatible clinical conditions with follow-up in 85 [pneumonia (n ⫽ 51), chronic resolving pneumonia (n ⫽ 20, resolution of lung consolidation ⬎ eight weeks), lung abscess (n ⫽ 12) and organized pneumonia (n ⫽ 2)]. Color Doppler ultrasound examination In the performance of color Doppler US examinations, a commercial color Doppler US equipment (Toshiba SSA-270A, Tokyo, Japan) with a 3.75 MHz convex probe was used to assess blood flows within thoracic lesions; since June 1999, another commercial color Doppler US equipment (Toshiba SSA-350A, Tokyo, Japan) has been used to assess the thoracic lesions. Both color Doppler US equipment (Toshiba SSA-270 and Toshiba SSA-350A) had the upgrade functions of conventional color Doppler US and power US (color angiography). In practice, power Doppler US has also been used to screen the thoracic lesions since June 1999, especially when vessel signals were not apparent by conventional color Doppler US. After obtaining informed consent from the patients and/or their families, patients were usually examined in a supine or prone position, but sometimes in a sitting position, according to the location of the thoracic lesions. Gray-scale US was first used to localize the lesions and then a color Doppler US examination was added. Before the start of the color Doppler US examination, the Doppler filter was usually set at 100 Hz to eliminate low-frequency signals from vessel wall motion and to avoid interference from respiratory and cardiac movement (Cosgrove et al. 1990; Hsu et al. 1998, 1996; Taylor et al. 1988; Yuan et al. 2000). Color Doppler gain was also adjusted until only a few noise specks were visible in the background (Cosgrove et al. 1990; Hsu et al. 1998, 1996). When color Doppler US
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
signals were detected, the sample volume was readjusted to approximate the size of detected blood vessels and the angle was repositioned to parallel the direction of blood flow (the Doppler angle between the ultrasound beam and flow signals was adjusted to obtain the largest frequency shift or velocity, as far below 60° as possible) (Hsu et al. 1996; Shimamoto et al. 1992). The pulse repetition frequency was also adjusted, depending on the blood flow velocity under investigation. The pulse-wave color Doppler US was used to detect the flow signals within thoracic lesions and all the Doppler signal waveforms were recorded on color-printed sonopaper and/or on a laser disk. Thus, all the data of the color Doppler US signals and spectral waveforms of the thoracic lesions could be reviewed and analyzed. In general, spectral waveforms that were reproducibly similar over three consecutive cardiac cycles were recorded as satisfactory (Hsu et al. 1998, 1996). Definition of a color Doppler US pulmonary artery vessel signal A pulsatile flow, with the vessel signal length on sonographic appearance ⱖ1 cm demonstrated smoothly by color Doppler US and waveform analysis, was arbitrarily defined as a pulmonary artery vessel signal. Using this color Doppler US vessel signal, thoracic lesions with at least a detectable pulmonary artery vessel signal were supposed to be benign. This hypothesis was based on the following findings: as shown in Figs. 1a, 1b, 1c and 1d, lung cancer is supplied by the bronchial artery, with the vessels within the lung cancer being torturous, small and irregular (without a predictable direction); moreover, pulmonary arteries are smooth, regular and predictable (Lyons and Vertova 1958; Ney et al. 1972; Viamonte 1965). Statistical analysis We collected and analyzed all pulsatile flow signals from the 264 thoracic lesions. Under the hypothesis of the color Doppler US pulmonary artery vessel signal being benign, we evaluated the value of color Doppler US pulmonary artery vessel signal sign to predict and differentiate benign lesions from lung cancers. As usual, we calculated the sensitivity, specificity, positive predictive value and negative predictive value of the color Doppler US pulmonary artery vessel signal to predict the benign lesions, using a chi-square test and p ⬍ 0.05 was considered to be significant. For a further judgment of clinical application value, we also used the likelihood ratio to assess the color Doppler US pulmonary artery vessel signal (Sackett et al. 2000).
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RESULTS Interpretation of color Doppler US pulsatile flow vessel signals and statistical analysis of the color Doppler US pulmonary artery vessel signal Among the 125 cytologically and/or histologically proven lung cancers, color Doppler US pulsatile flow vessel signals were detected in a total of 73 (58%), including the major cell types of squamous cell carcinoma (36, 58%), adenocarcinoma (23, 61%) and small cell carcinoma (9, 64%). The remaining minor cell types of carcinoma also had detectable color Doppler US pulsatile flow vessel signals in five (38%). Of these, the color Doppler US pulmonary artery vessel signal was found in only two (2%) lung cancers of specific alveolar cell carcinoma with lobar consolidation. In the 139 clinically compatible benign lesions, color Doppler US pulsatile flow vessel signals were detected in a total of 107 (77%), including the major different diseases of 43 (84%) pneumonia, 17 (85%) chronic resolving pneumonia, 15 (68%) lung abscess, 10 (83%) exudative tuberculous pneumonia and six (60%) cryptococcosis. The remaining different benign diseases also had color Doppler US pulsatile flow vessel signals present in 16 (67%), ranging in percentages from 0% to 100%. Of these, the color Doppler US pulmonary artery vessel signal was present in a total of 74 (53%) benign lesions. Interestingly, we also found that five patients (four pulmonary sequestration and one congenital cystic adenomatoid malformation) had the prominent color Doppler US pulsatile flow vessel signals; however, we believe that these five patients’ prominent color Doppler US pulsatile flow vessel signals were representative of systemic arteries (color Doppler US pseudo-pulmonary artery vessel signal) and did not emanate from pulmonary arteries. Table 1 shows the results in detail. Using the color Doppler US pulmonary artery vessel signal, color Doppler US is valuable in predicting and differentiating benign lesions from lung cancers (p ⬍ 0.0001, sensitivity ⫽ 0.53, specificity ⫽ 0.98, positive predictive value ⫽ 0.97, negative predictive value ⫽ 0.65 and positive likelihood ratio 26.5). As mentioned above, five benign lesions (four pulmonary sequestration and one congenital cystic adenomatoid malformation) might have had detectable color Doppler US pseudo-pulmonary artery vessel signals, which were still representative of benign lesions. The clinical application of the color Doppler US pulmonary artery vessel signal is demonstrated in the following case reports. Illustrative cases Patient 1. A 65-y-old man was admitted to our hospital due to dull pain in the right chest for two weeks.
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Fig. 1. This patient was a 46-y-old man with intermittent hemoptysis for several months. (a) Chest radiography showed a mass in the left upper lobe. Squamous cell carcinoma was diagnosed by ultrasound-guided fine needle aspiration. (b) Bronchial arteriogram showed the tumor was supplied by the bronchial arteries, which originated from the same level of the right bronchial artery. However, the vessels within the tumor were torturous, small and irregular (without predictable direction). (c) Color Doppler US demonstrated only a small short segment of pulsatile flows within the tumor. (d) Pulmonary angiogram showed the pulmonary arteries running smoothly and regularly.
Chest radiography showed a mass-like lesion in the right middle lung field (Fig. 2a). Because there were no infectious symptoms and signs, the first impression was of lung cancer. Gray-scale US showed only a hypoechoic lesion without apparent air-bronchograms. Nevertheless,
color Doppler US revealed a pulsatile flow vessel signal within the lesion, with the pulmonary artery vessel signal present (Fig. 2b). Thus, oral antibiotic was prescribed and the lung lesion completely resolved within two weeks after admission.
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
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Table 1. Color Doppler Ultrasound Examinations with Present Pulsatile Flow Signals and Pulmonary Artery Vessel Signals in 264 Thoracic Lesions
Underlying disease
No. of lesions
No. of pulsatile flow signals present [n (%)]
No. of pulmonary artery vessel signal signs [n (%)]
62 38 14 4 2 5 125
36 (58) 23 (61) 9 (64) 0 (0) 2 (100) 3 (100) 73 (58)
0 (0) 2 (5)‡ 0 (0) 0 (0) 0 (0) 0 (0) 2 (2)†
51 20 22 10 12 4 3 5 3 4 1 3 1 139
43 (84) 17 (85) 15 (68) 6 (60) 10 (83) 0 (0) 2 (67) 3 (60) 2 (67) 4 (100) 1 (100) 3 (100) 1 (100) 107 (77)
28 (55) 14 (70) 9 (41) 4 (40) 6 (50) 0 (0) 2 (67) 1 (20) 1 (33) 4 (100)* 1 (100) 3 (100) 1 (100)* 74 (53)†
Lung cancers Squamous cell carcinoma Adenocarcinoma Small cell lung cancer Adenosquamous carcinoma Large cell carcinoma Carcinoma, poorly differentiated (non-SCLC type) Total Benign lesions Pneumonia Chronic resolving pneumonia Lung abscess Cryptococcosis Exudative tuberculous pneumonia Tuberculoma Tuberculous granulomatous Inflammation Organized pneumonia Actinomycosis Pulmonary sequestration Mucormycosis Nocardiosis Congenital cystic adenomatoid malformation Total SCLC ⫽ small cell lung cancer.
† p ⬍ 0.0001 by chi-square test. ‡ Specific alveolar cell carcinoma with lobar consolidation. * Pseudo-pulmonary artery vessel signal.
Patient 2. This 42-y-old man was admitted to our hospital due to a chronic cough for several months. Chest radiography showed a patchy consolidation in the right lower lung field (Fig. 3a). After admission, a series of conventional examinations was performed, including sputum cytology, fiberoptic bronchoscopy, thoracic CT scan and US-guided percutaneous needle aspiration; however, no confirmed diagnosis was made. Color Doppler US examination revealed a pulsatile flow, with the presence of pulmonary artery vessel signal (Fig. 3b). Although a benign lesion was suggested, the patient still underwent a surgical resection due to an unknown diagnosis and a lingering suspicion of lung cancer. The corresponding pulmonary artery was found in the resected specimen and the final diagnosis was cryptococcosis. Patient 3. A 62-y-old patient was referred to our hospital due to fever, right chest pain and cough with blood-tinged sputum lasting for several days. The chest radiograph showed lobar consolidation in the right middle lobe with some pleural effusion (Fig. 4a). After admission, a chest US examination was performed and gray-scale chest US revealed a slightly hyperechoic mass (arrowheads) surrounded by a hypoechoic lesion in the peripheral region (Fig. 4b). Lung cancer with obstructive
pneumonitis was suspected, due to a mass-like lesion and a lack of apparent air-bronchograms by the sonographic appearance. However, power Doppler US revealed the vessel signals prominently and there was a detectable pulmonary artery vessel signal found by waveform analysis (Fig. 4c). Thus, pneumonia was again the first impression and, initially, intravenous antibiotics were given for one week. Although the follow-up chest radiograph still showed a well-defined large mass lesion (Fig. 4d), oral antibiotic was prescribed for another two weeks in the outpatient department. With continuous follow-up, the chronic resolving pneumonia had almost completely resolved three months later. Patient 4. This 75-y-old male visited our hospital due to cough with scanty sputum, poor appetite and body weight loss for several weeks. The chest radiograph revealed fibroproductive infiltrations in the bilateral upper lung fields (Fig. 5a). The patient then received chemotherapy for tuberculosis for about one month. However, the patient’s condition did not improve and the follow-up chest radiograph showed a large mass with cavitation in the left upper lobe (Fig. 5b). The thoracic CT scan also clearly demonstrated central necrosis in the upper portion of the mass lesion (Fig. 5c). Clinically, lung cancer was highly suspected, by evidence from the
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examination, the sputum culture for tuberculosis was reported to be positive. The patient’s condition also improved after a six-month treatment for tuberculosis, with only residual lesions on his follow-up chest radiograph.
Fig. 2. (a) Chest radiography showed a mass-like lesion in the right middle lung field. (b) Color Doppler US revealed a pulsatile flow within the lesion with the pulmonary artery vessel signal present.
chest radiographs and thoracic CT scan examination. Gray-scale US showed a well-defined mass-like lesion at the left upper lobe (Fig. 5d), but power Doppler US easily demonstrated prominent vessel signals with the pulmonary artery vessel signal in waveform analysis (Fig. 5e). The patient continued to receive the chemotherapy for tuberculosis. Three weeks after the chest US
Fig. 3. (a) Chest radiography showed a consolidation in the right lower lung field. (b) Color Doppler US also revealed a pulsatile flow within the lesion, with the pulmonary artery vessel signal present. However, the patient still received a surgical resection due to an unknown diagnosis and a suspicion of lung cancer. The corresponding pulmonary artery was found in the resected histologic specimen and pulmonary cryptococcosis was proven.
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
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Fig. 4. (a) Chest radiograph showed lobar consolidation in the right middle lobe with some pleural effusion. (b) Gray-scale chest US revealed a slightly hyperechoic mass (arrowheads) surrounded by a hypoechoic lesion in the peripheral region. Lung cancer with obstructive pneumonitis was suspected. (c) Power Doppler US clearly demonstrated prominent vessel signals, with the pulmonary artery vessel signal by waveform analysis. Pneumonia was again the first impression. (d) The follow-up chest radiograph showed a well-defined mass-like lesion after antibiotic treatment for several days. With continuing oral antibiotic treatment for two weeks and careful follow-up in the outpatient department, the chronic resolving pneumonia was almost completely resolved three months later.
Patient 5. This 54-y-old female had chronic cough with whitish sputum for several years. On admission, the chest radiograph showed lobar consolidation in the left lower lobe and some nodules in the right lower lobe. The thoracic CT scan revealed consolidation in the left lower lobe with CT-angiogram signs present (Fig. 6a). Color Doppler US also demonstrated a mass lesion with the pulmonary artery vessel signal sign present (Fig. 6b). Alveolar cell carcinoma was proven by US-guided fine needle aspiration biopsy and surgical resection. This is one of the exceptions in specific consolidation type al-
veolar cell carcinoma with lobar consolidation and a color Doppler US pulmonary artery vessel signal sign present. DISCUSSION Of the imaging examinations (chest radiograph, CT, US, magnetic resonance imaging, angiography and fluoroscopy) used in chest medicine, color Doppler US is the only imaging modality capable of easily and conveniently assessing the vessel signals in peripheral pulmo-
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Fig. 5. (a) Chest radiograph showed fibroproductive infiltrations in the bilateral upper lung fields and active pulmonary tuberculosis was considered. (b) After the chemotherapy for tuberculosis lasting one month, the chest radiograph showed a large mass with cavitation in the left upper lobe. (c) Thoracic CT scan also clearly demonstrated central necrosis in the mass lesion. Clinically, lung cancer was highly suspected. (d) Gray-scale US also revealed a well-defined mass-like lesion at the left upper lobe. (e) However, power Doppler US could easily demonstrate the prominent vessels with the pulmonary artery vessel signal, using waveform analysis. After continuing chemotherapy for tuberculosis for six months, the patient’s condition improved, with only residual lesions on his follow-up chest radiograph.
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
Fig. 6. (a) Thoracic CT scan revealed consolidation in the left lower lobe with CT-angiogram signs present. (b) Color Doppler US also showed a large mass with color Doppler US pulmonary artery vessel signals. Alveolar cell carcinoma was confirmed by US-guided fine needle aspiration biopsy and surgical resection. This is one exception, in which the color Doppler US pulmonary artery vessel signal was present in specific alveolar cell carcinoma with lobar consolidation.
nary lesions. In our experience, color Doppler US can not only detect the tumor vessel signals in lung cancers, but can also easily predict and confirm pulmonary benign lesions, using the pulmonary artery vessel signal, with high specificity and without any risk (Hsu et al. 1996). Practically, when focusing on the screening for the color Doppler US pulmonary artery vessel signal, the color Doppler US examination is always accomplished within 10 min. This simple technique can eliminate the need for some patients with thoracic lesions mimicking lung cancers (e.g., chronic resolving pneumonia, lung abscesses, fungal infections, tuberculous granulomatous inflammation, organized pneumonia etc.) to undergo immediate semi-invasive or invasive diagnostic procedures, such as thoracoscopic biopsy, surgical resection etc.
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Why did we define the pulsatile flow vessel signal length on sonographic appearance ⱖ1 cm demonstrated by color Doppler US as a pulmonary artery vessel signal? How is the definition of color Doppler US pulmonary artery vessel signal ⱖ0.5 cm or 1.5 cm? As we know, pulmonary benign lesions may have smooth blood supply from both pulmonary arteries and bronchial arteries (Gorg et al. 2003; Hsu et al. 1998, 1996). Although the prominent vessel signals demonstrated by color Doppler US are almost all from pulmonary arteries, a small pulsatile flow with the vessel signal length on sonographic appearance ⱖ0.5 cm demonstrated by color Doppler US may be representative of pulmonary artery or bronchial artery. Thus, the differentiation between pulmonary artery or bronchial artery by using a small pulsatile flow with the vessel signal length ⱖ0.5 cm on sonographic appearance by color Doppler US is somewhat difficult. Why did we not define the vessel signal length ⱖ1.5 cm on sonographic appearance as the color Doppler US pulmonary artery vessel signal? In our series, some benign lesions had the lesion size ⱕ3 cm in diameter, which is often difficult to demonstrate the color Doppler US pulmonary artery vessel signal ⱖ1.5 cm on sonographic appearance (Fig. 2). Practically, color Doppler US pulmonary artery vessel signal ⱖ1.5 cm were always detected in pulmonary lesions ⱖ4 cm in diameter in our series. Based on above findings and our initial experience, we defined the pulsatile flow with the vessel signal length ⱖ1 cm on sonographic appearance demonstrated by color Doppler US as the color Doppler US pulmonary artery vessel signal. In our more than 6 y experience using the color Doppler US pulmonary artery vessel signal to predict the benign lesions, there has been only one exception (as shown in Fig. 6) in which alveolar cell carcinoma presenting as pulmonary lobar consolidation had a pulmonary artery vessel signal. Alveolar cell carcinoma may have the specific CT angiogram sign, which is thought to be due to pulmonary arteries running through the cancer and is specific among the lung cancers presenting with pulmonary consolidations (IM et al. 1990). Clinically, among 125 lung cancers, we have indeed encountered two patients with alveolar cell carcinoma with lobar consolidation presenting with a color Doppler US pulmonary artery vessel signal. Nevertheless, for an experienced physician with expertise in chest US, gray-scale US can easily diagnose alveolar cell carcinoma with lobar consolidation as lung cancer, using the image alone. In addition to lung cancer, we have performed color Doppler US examinations with nine other pulmonary malignancies, including two malignant lymphoma and seven metastatic lung cancers [cervical cancer (n ⫽ 2), endometrial cancer (n ⫽ 1), transitional cell carcinoma of the bladder (n ⫽ 1), colon cancer (n ⫽ 1), nasopharyngeal cancer (n ⫽ 1) and osteogenic sarcoma of the left
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femur (n ⫽ 1)]. Of these, five had detectable color Doppler US pulsatile flow vessel signals [cervical cancer (n ⫽ 1), endometrial cancer (n ⫽ 1), transitional cell carcinoma of bladder (n ⫽ 1), nasopharyngeal cancer (n ⫽ 1) and malignant lymphoma (n ⫽ 1)], but still had no color Doppler US pulmonary artery vessel signal present. Although we had short experience and did not perform pulmonary and bronchial angiograms for metastatic lung cancers, we believe that the color Doppler US pulmonary artery vessel signal could also be used with pulmonary benign lesions to exclude the possibility of metastatic lung cancers. Undoubtedly, the application of the color Doppler US pulmonary artery vessel signal to exclude other pulmonary malignancies warrants a further largerscale study in the future. In other congenital or chronic infectious lung diseases, such as bronchiectasis with organizing pneumonia, pulmonary sequestration, congenital cystic adenomatoid malformation etc., the color Doppler US pulmonary artery vessel signal is often present. However, the detected and prominent pulsatile flow vessel signals may originate from the systemic arteries, not from the pulmonary arteries; in this situation, as shown in Table 1, we called these vessel signals pseudo-pulmonary artery vessel signals (Hernanz-Schulman et al. 1991). Nevertheless, both the color Doppler US pulmonary artery vessel signal and the pseudo-pulmonary artery vessel signal still imply that the pulmonary lesions are benign. Certainly, color Doppler US has some limitations and influencing factors in the detection of vessel signals of thoracic lesions, such as the insonating angle, flow velocity, US probe, anatomic narrowing interface and the necessity for the patient’s cooperation. Moreover, only abutting chest wall lesions can possibly be examined by color Doppler US. Of these, the limitation of detecting slow flow vessels and the influence of the insonating angle are the main concerns of conventional color Doppler US. Nevertheless, there is no doubt that prominent vessels can be easily detected by conventional color Doppler US. Regarding the detection of low-flow vessel signals and the influence of the insonating angle (the Doppler angle : between the ultrasound beam and the flow vessel signals), high-end advanced US equipment and functions have overcome some these limitations (Bude et al. 1994; Rubin et al. 1994). Thus, we believe that rapid improvements in ultrasound equipment and advances in biological technology will broaden the clinical application of color Doppler US. As shown in Fig. 5, we believe the added application of power Doppler US will also significantly increase the sensitivity of color Doppler US to detect the pulmonary artery vessel signal (Bude et al. 1994; Rubin et al. 1994). In conclusion, color Doppler US is helpful in assessing vessel signals in thoracic lesions and the appli-
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cation of the color Doppler US pulmonary artery vessel signal sign is valuable in predicting and differentiating pulmonary benign lesions from lung cancers, with high specificity and without any risk. It is worthy of being widely used in chest medicine, especially with thoracic lesions mimicking lung cancers and without a conclusive diagnosis by conventional examinations. Moreover, it is usually accomplished within 10 min and can lead to the avoidance of some unnecessary semiinvasive or invasive diagnostic procedures. Acknowledgements—This study was supported in part by research grant 13401 from Department of Health, Executive Yuan, Taiwan.
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doi:10.1016/j.ultrasmedbio.2006.08.011
● Original Contribution COLOR DOPPLER US PULMONARY ARTERY VESSEL SIGNAL: A SIGN FOR PREDICTING THE BENIGN LESIONS WU-HUEI HSU,* YANG-HAO YU,* CHIH-YEN TU,* JEN-YUAN HSU† CHIH-YI CHEN,‡ CHUN-LIEH CHEN,§ and PO-CHEUNG KWAN㛳 *Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan; Divisions of †Pulmonary and Critical Care Medicine and ‡Thoracic Surgery, Departments of †Internal Medicine, ‡Surgery, and 㛳Pathology, Taichung Veterans General Hospital, Taichung, Taiwan; and §Division of Thoracic Surgery, Department of Surgery, Feng-Yuan Hospital, Department of Health, Executive Yuan, Taiwan. (Received 12 April 2006, revised 8 August 2006, in final form 17 August 2006)
Abstract—The lung cancer blood supply originates from the bronchial artery. If vessel signals within pulmonary lesions can be confirmed to be those of the pulmonary artery, color Doppler ultrasound (US) should be able to predict and differentiate benign lesions from lung cancers. Two hundred sixty-four patients with abutting thoracic lesions (including 125 lung cancers and 139 benign lesions) underwent color Doppler US examinations. A pulsatile flow, with the vessel signal length on sonographic appearance >1 cm demonstrated by color Doppler US, was arbitrarily defined as a pulmonary artery vessel signal. Of the 264 thoracic lesions, 73 (58%) lung cancers and 107 (77%) benign lesions had detectable color Doppler US pulsatile flow vessel signals. Analyzing the pulsatile flow vessel signals, the color Doppler US pulmonary artery vessel signal was present in 74 (53%) benign lesions, but was found in only two (2%) lung cancers of a specific alveolar cell carcinoma with lobar consolidation. Using the pulmonary artery vessel signal, color Doppler US can be valuable in predicting and differentiating benign lesions from lung cancers (p < 0.0001, sensitivity ⴝ 0.53, specificity ⴝ 0.98 and positive likelihood ratio 26.5). In conclusion, color Doppler US pulmonary artery vessel signal sign is useful in predicting and differentiating benign lesions from lung cancers. (E-mail: [email protected]) © 2007 World Federation for Ultrasound in Medicine & Biology. Key Words: Ultrasonography, Doppler, Lung, Vessel, Neoplasm.
mimicking lung cancers, some semi-invasive or invasive procedures, such as thoracoscopic biopsy or surgical resection, are sometimes necessary to make a confirmative diagnosis and to exclude the possibility of lung cancers. Lung cancers are always supplied by the bronchial artery system. Thus, previously pulmonary and bronchial angiograms were used to diagnose and differentiate lung cancers from benign lesions (Lyons and Vertova 1958; Ney et al. 1972; Viamonte 1965). Among the imaging modalities used in chest medicine, color Doppler ultrasound (US) has been applied to assess the vessel signals in thoracic lesions (Gorg et al. 2003; Gorguner et al. 2003; Hsu et al. 1998, 1996; Yuan et al. 2000). Thus, from our viewpoint and experience, color Doppler US, being able to assess the vessel signals of thoracic lesions, should be able to predict and differentiate benign lesions from lung cancers.
INTRODUCTION Image [fluoroscopy, computed tomography (CT), ultrasound (US)]-guided percutaneous transthoracic needle biopsy is a well-documented technique for diagnosing thoracic tumors (Ikezoe et al. 1990; Yang et al. 1992). For malignant tumors or lung cancers, the diagnostic yields of image-guided percutaneous transthoracic needle biopsy are all ⱖ90% in published papers (Ikezoe et al. 1990; Yang et al. 1992). Nevertheless, some pulmonary benign lesions are difficult to diagnose accurately by image examinations alone and/or by image-guided percutaneous needle biopsy. Clinically, it is very important to determine the nature of thoracic lesions to make an appropriate therapeutic decision. Therefore, in the case of benign pulmonary lesions, especially lesions Address correspondence to: Dr. Wu-Huei Hsu, MD, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan. E-mail: [email protected] 379
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Herein, we describe our findings regarding the clinical application of the color Doppler US pulmonary artery vessel signal. Color Doppler US pulmonary artery vessel signal is defined as a pulsatile flow, with the vessel signal length on sonographic appearance ⱖ1 cm demonstrated smoothly by color Doppler US. Using this pulmonary artery vessel signal, color Doppler US can easily and quickly predict and differentiate pulmonary benign lesions from lung cancers with high specificity and without any risk. MATERIALS AND METHODS Patients From April 1994 to November 2001, 264 patients with thoracic lesions abutting chest wall, confirmed diagnoses and compatible clinical conditions during follow-up undergoing color Doppler US examinations were enrolled in our series. The examined patients included 207 men and 57 women, ranging in age from 17 to 88 y (mean ⫽ 58). The final diagnoses consisted of lung cancers in 125 patients and benign lesions in 139 patients. The sizes of the lung cancers, by calculating the diameter from chest radiographs, ranged from 2.0 to 13.0 cm, with a mean of 6.5 ⫾ 2.4 cm; and the sizes of the benign lesions ranged from 1.7 to 12.0 cm, with a mean of 6.9 ⫾ 2.5 cm. The proven cytologic and/or histologic diagnoses of the 125 lung cancers were squamous cell carcinoma (n ⫽ 62), adenocarcinoma (n ⫽ 38), small cell carcinoma (n ⫽ 14), adenosquamous carcinoma (n ⫽ 4), large cell carcinoma (n ⫽ 2) and poorly differentiated carcinoma (n ⫽ 5, non-small cell lung cancer type). The diagnoses of lung cancers were made by the following methods: US-guided needle biopsy (n ⫽ 98), transbronchial biopsy (n ⫽ 21), lymph node aspiration or surgical biopsy (n ⫽ 6), surgical resection (n ⫽ 38, including craniotomy in one) and sputum cytology (n ⫽ 6). Of these, 38 patients had a positive cytologic and/or histologic diagnosis made by two or more of the examinations listed above. Among the 125 patients with proven lung cancers, four were initially diagnosed as squamous cell carcinoma (n ⫽ 3) and adenocarcinoma (n ⫽ 1) by US-guided fine needle aspiration biopsy; however, a final diagnosis of adenosquamous carcinoma was confirmed by surgical resection. Another two were also misdiagnosed as poorly differentiated squamous cell carcinoma by US-guided fine needle aspiration biopsy, but adenocarcinoma was proven by US-guided large-bore cutting biopsy (n ⫽ 1) and surgical resection (n ⫽ 1). The diagnoses of the 139 benign lesions were made by the following methods: surgical resection in 16 [tuberculoma (n ⫽ 4), cryptococcosis (n ⫽ 2), organized
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pneumonia (n ⫽ 3), pulmonary sequestration (n ⫽ 4), mucormycosis (n ⫽ 1), actinomycosis (n ⫽ 1) and congenital cystic adenomatoid malformation (n ⫽ 1)]; USguided fine needle aspiration with positive causative microorganisms in 17 [lung abscess (n ⫽ 8), cryptococcosis (n ⫽ 6), actinomycosis (n ⫽ 2) and tuberculous granulomatous inflammation (n ⫽ 1)]; US-guided fine needle aspiration and surgical resection in two (cryptococcosis, progressive change in the lung lesions in spite of medical managements), positive causative microorganisms in two [lung abscesses, by transbronchial brush (n ⫽ 1) and blood culture (n ⫽ 1)]; exudative tuberculous pneumonia with confirmed diagnoses and compatible clinical conditions during follow-up in 12 [positive sputum acid-fast stain and culture (n ⫽ 5), positive sputum culture (n ⫽ 6) and pleural biopsy (n ⫽ 1)]; tuberculous granulomatous inflammation with compatible clinical condition in two [positive sputum acid-fast stain (n ⫽ 1) and sputum culture (n ⫽ 1)]; nocardiosis with positive sputum gram stain in three and compatible clinical conditions with follow-up in 85 [pneumonia (n ⫽ 51), chronic resolving pneumonia (n ⫽ 20, resolution of lung consolidation ⬎ eight weeks), lung abscess (n ⫽ 12) and organized pneumonia (n ⫽ 2)]. Color Doppler ultrasound examination In the performance of color Doppler US examinations, a commercial color Doppler US equipment (Toshiba SSA-270A, Tokyo, Japan) with a 3.75 MHz convex probe was used to assess blood flows within thoracic lesions; since June 1999, another commercial color Doppler US equipment (Toshiba SSA-350A, Tokyo, Japan) has been used to assess the thoracic lesions. Both color Doppler US equipment (Toshiba SSA-270 and Toshiba SSA-350A) had the upgrade functions of conventional color Doppler US and power US (color angiography). In practice, power Doppler US has also been used to screen the thoracic lesions since June 1999, especially when vessel signals were not apparent by conventional color Doppler US. After obtaining informed consent from the patients and/or their families, patients were usually examined in a supine or prone position, but sometimes in a sitting position, according to the location of the thoracic lesions. Gray-scale US was first used to localize the lesions and then a color Doppler US examination was added. Before the start of the color Doppler US examination, the Doppler filter was usually set at 100 Hz to eliminate low-frequency signals from vessel wall motion and to avoid interference from respiratory and cardiac movement (Cosgrove et al. 1990; Hsu et al. 1998, 1996; Taylor et al. 1988; Yuan et al. 2000). Color Doppler gain was also adjusted until only a few noise specks were visible in the background (Cosgrove et al. 1990; Hsu et al. 1998, 1996). When color Doppler US
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
signals were detected, the sample volume was readjusted to approximate the size of detected blood vessels and the angle was repositioned to parallel the direction of blood flow (the Doppler angle between the ultrasound beam and flow signals was adjusted to obtain the largest frequency shift or velocity, as far below 60° as possible) (Hsu et al. 1996; Shimamoto et al. 1992). The pulse repetition frequency was also adjusted, depending on the blood flow velocity under investigation. The pulse-wave color Doppler US was used to detect the flow signals within thoracic lesions and all the Doppler signal waveforms were recorded on color-printed sonopaper and/or on a laser disk. Thus, all the data of the color Doppler US signals and spectral waveforms of the thoracic lesions could be reviewed and analyzed. In general, spectral waveforms that were reproducibly similar over three consecutive cardiac cycles were recorded as satisfactory (Hsu et al. 1998, 1996). Definition of a color Doppler US pulmonary artery vessel signal A pulsatile flow, with the vessel signal length on sonographic appearance ⱖ1 cm demonstrated smoothly by color Doppler US and waveform analysis, was arbitrarily defined as a pulmonary artery vessel signal. Using this color Doppler US vessel signal, thoracic lesions with at least a detectable pulmonary artery vessel signal were supposed to be benign. This hypothesis was based on the following findings: as shown in Figs. 1a, 1b, 1c and 1d, lung cancer is supplied by the bronchial artery, with the vessels within the lung cancer being torturous, small and irregular (without a predictable direction); moreover, pulmonary arteries are smooth, regular and predictable (Lyons and Vertova 1958; Ney et al. 1972; Viamonte 1965). Statistical analysis We collected and analyzed all pulsatile flow signals from the 264 thoracic lesions. Under the hypothesis of the color Doppler US pulmonary artery vessel signal being benign, we evaluated the value of color Doppler US pulmonary artery vessel signal sign to predict and differentiate benign lesions from lung cancers. As usual, we calculated the sensitivity, specificity, positive predictive value and negative predictive value of the color Doppler US pulmonary artery vessel signal to predict the benign lesions, using a chi-square test and p ⬍ 0.05 was considered to be significant. For a further judgment of clinical application value, we also used the likelihood ratio to assess the color Doppler US pulmonary artery vessel signal (Sackett et al. 2000).
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RESULTS Interpretation of color Doppler US pulsatile flow vessel signals and statistical analysis of the color Doppler US pulmonary artery vessel signal Among the 125 cytologically and/or histologically proven lung cancers, color Doppler US pulsatile flow vessel signals were detected in a total of 73 (58%), including the major cell types of squamous cell carcinoma (36, 58%), adenocarcinoma (23, 61%) and small cell carcinoma (9, 64%). The remaining minor cell types of carcinoma also had detectable color Doppler US pulsatile flow vessel signals in five (38%). Of these, the color Doppler US pulmonary artery vessel signal was found in only two (2%) lung cancers of specific alveolar cell carcinoma with lobar consolidation. In the 139 clinically compatible benign lesions, color Doppler US pulsatile flow vessel signals were detected in a total of 107 (77%), including the major different diseases of 43 (84%) pneumonia, 17 (85%) chronic resolving pneumonia, 15 (68%) lung abscess, 10 (83%) exudative tuberculous pneumonia and six (60%) cryptococcosis. The remaining different benign diseases also had color Doppler US pulsatile flow vessel signals present in 16 (67%), ranging in percentages from 0% to 100%. Of these, the color Doppler US pulmonary artery vessel signal was present in a total of 74 (53%) benign lesions. Interestingly, we also found that five patients (four pulmonary sequestration and one congenital cystic adenomatoid malformation) had the prominent color Doppler US pulsatile flow vessel signals; however, we believe that these five patients’ prominent color Doppler US pulsatile flow vessel signals were representative of systemic arteries (color Doppler US pseudo-pulmonary artery vessel signal) and did not emanate from pulmonary arteries. Table 1 shows the results in detail. Using the color Doppler US pulmonary artery vessel signal, color Doppler US is valuable in predicting and differentiating benign lesions from lung cancers (p ⬍ 0.0001, sensitivity ⫽ 0.53, specificity ⫽ 0.98, positive predictive value ⫽ 0.97, negative predictive value ⫽ 0.65 and positive likelihood ratio 26.5). As mentioned above, five benign lesions (four pulmonary sequestration and one congenital cystic adenomatoid malformation) might have had detectable color Doppler US pseudo-pulmonary artery vessel signals, which were still representative of benign lesions. The clinical application of the color Doppler US pulmonary artery vessel signal is demonstrated in the following case reports. Illustrative cases Patient 1. A 65-y-old man was admitted to our hospital due to dull pain in the right chest for two weeks.
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Fig. 1. This patient was a 46-y-old man with intermittent hemoptysis for several months. (a) Chest radiography showed a mass in the left upper lobe. Squamous cell carcinoma was diagnosed by ultrasound-guided fine needle aspiration. (b) Bronchial arteriogram showed the tumor was supplied by the bronchial arteries, which originated from the same level of the right bronchial artery. However, the vessels within the tumor were torturous, small and irregular (without predictable direction). (c) Color Doppler US demonstrated only a small short segment of pulsatile flows within the tumor. (d) Pulmonary angiogram showed the pulmonary arteries running smoothly and regularly.
Chest radiography showed a mass-like lesion in the right middle lung field (Fig. 2a). Because there were no infectious symptoms and signs, the first impression was of lung cancer. Gray-scale US showed only a hypoechoic lesion without apparent air-bronchograms. Nevertheless,
color Doppler US revealed a pulsatile flow vessel signal within the lesion, with the pulmonary artery vessel signal present (Fig. 2b). Thus, oral antibiotic was prescribed and the lung lesion completely resolved within two weeks after admission.
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
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Table 1. Color Doppler Ultrasound Examinations with Present Pulsatile Flow Signals and Pulmonary Artery Vessel Signals in 264 Thoracic Lesions
Underlying disease
No. of lesions
No. of pulsatile flow signals present [n (%)]
No. of pulmonary artery vessel signal signs [n (%)]
62 38 14 4 2 5 125
36 (58) 23 (61) 9 (64) 0 (0) 2 (100) 3 (100) 73 (58)
0 (0) 2 (5)‡ 0 (0) 0 (0) 0 (0) 0 (0) 2 (2)†
51 20 22 10 12 4 3 5 3 4 1 3 1 139
43 (84) 17 (85) 15 (68) 6 (60) 10 (83) 0 (0) 2 (67) 3 (60) 2 (67) 4 (100) 1 (100) 3 (100) 1 (100) 107 (77)
28 (55) 14 (70) 9 (41) 4 (40) 6 (50) 0 (0) 2 (67) 1 (20) 1 (33) 4 (100)* 1 (100) 3 (100) 1 (100)* 74 (53)†
Lung cancers Squamous cell carcinoma Adenocarcinoma Small cell lung cancer Adenosquamous carcinoma Large cell carcinoma Carcinoma, poorly differentiated (non-SCLC type) Total Benign lesions Pneumonia Chronic resolving pneumonia Lung abscess Cryptococcosis Exudative tuberculous pneumonia Tuberculoma Tuberculous granulomatous Inflammation Organized pneumonia Actinomycosis Pulmonary sequestration Mucormycosis Nocardiosis Congenital cystic adenomatoid malformation Total SCLC ⫽ small cell lung cancer.
† p ⬍ 0.0001 by chi-square test. ‡ Specific alveolar cell carcinoma with lobar consolidation. * Pseudo-pulmonary artery vessel signal.
Patient 2. This 42-y-old man was admitted to our hospital due to a chronic cough for several months. Chest radiography showed a patchy consolidation in the right lower lung field (Fig. 3a). After admission, a series of conventional examinations was performed, including sputum cytology, fiberoptic bronchoscopy, thoracic CT scan and US-guided percutaneous needle aspiration; however, no confirmed diagnosis was made. Color Doppler US examination revealed a pulsatile flow, with the presence of pulmonary artery vessel signal (Fig. 3b). Although a benign lesion was suggested, the patient still underwent a surgical resection due to an unknown diagnosis and a lingering suspicion of lung cancer. The corresponding pulmonary artery was found in the resected specimen and the final diagnosis was cryptococcosis. Patient 3. A 62-y-old patient was referred to our hospital due to fever, right chest pain and cough with blood-tinged sputum lasting for several days. The chest radiograph showed lobar consolidation in the right middle lobe with some pleural effusion (Fig. 4a). After admission, a chest US examination was performed and gray-scale chest US revealed a slightly hyperechoic mass (arrowheads) surrounded by a hypoechoic lesion in the peripheral region (Fig. 4b). Lung cancer with obstructive
pneumonitis was suspected, due to a mass-like lesion and a lack of apparent air-bronchograms by the sonographic appearance. However, power Doppler US revealed the vessel signals prominently and there was a detectable pulmonary artery vessel signal found by waveform analysis (Fig. 4c). Thus, pneumonia was again the first impression and, initially, intravenous antibiotics were given for one week. Although the follow-up chest radiograph still showed a well-defined large mass lesion (Fig. 4d), oral antibiotic was prescribed for another two weeks in the outpatient department. With continuous follow-up, the chronic resolving pneumonia had almost completely resolved three months later. Patient 4. This 75-y-old male visited our hospital due to cough with scanty sputum, poor appetite and body weight loss for several weeks. The chest radiograph revealed fibroproductive infiltrations in the bilateral upper lung fields (Fig. 5a). The patient then received chemotherapy for tuberculosis for about one month. However, the patient’s condition did not improve and the follow-up chest radiograph showed a large mass with cavitation in the left upper lobe (Fig. 5b). The thoracic CT scan also clearly demonstrated central necrosis in the upper portion of the mass lesion (Fig. 5c). Clinically, lung cancer was highly suspected, by evidence from the
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examination, the sputum culture for tuberculosis was reported to be positive. The patient’s condition also improved after a six-month treatment for tuberculosis, with only residual lesions on his follow-up chest radiograph.
Fig. 2. (a) Chest radiography showed a mass-like lesion in the right middle lung field. (b) Color Doppler US revealed a pulsatile flow within the lesion with the pulmonary artery vessel signal present.
chest radiographs and thoracic CT scan examination. Gray-scale US showed a well-defined mass-like lesion at the left upper lobe (Fig. 5d), but power Doppler US easily demonstrated prominent vessel signals with the pulmonary artery vessel signal in waveform analysis (Fig. 5e). The patient continued to receive the chemotherapy for tuberculosis. Three weeks after the chest US
Fig. 3. (a) Chest radiography showed a consolidation in the right lower lung field. (b) Color Doppler US also revealed a pulsatile flow within the lesion, with the pulmonary artery vessel signal present. However, the patient still received a surgical resection due to an unknown diagnosis and a suspicion of lung cancer. The corresponding pulmonary artery was found in the resected histologic specimen and pulmonary cryptococcosis was proven.
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
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Fig. 4. (a) Chest radiograph showed lobar consolidation in the right middle lobe with some pleural effusion. (b) Gray-scale chest US revealed a slightly hyperechoic mass (arrowheads) surrounded by a hypoechoic lesion in the peripheral region. Lung cancer with obstructive pneumonitis was suspected. (c) Power Doppler US clearly demonstrated prominent vessel signals, with the pulmonary artery vessel signal by waveform analysis. Pneumonia was again the first impression. (d) The follow-up chest radiograph showed a well-defined mass-like lesion after antibiotic treatment for several days. With continuing oral antibiotic treatment for two weeks and careful follow-up in the outpatient department, the chronic resolving pneumonia was almost completely resolved three months later.
Patient 5. This 54-y-old female had chronic cough with whitish sputum for several years. On admission, the chest radiograph showed lobar consolidation in the left lower lobe and some nodules in the right lower lobe. The thoracic CT scan revealed consolidation in the left lower lobe with CT-angiogram signs present (Fig. 6a). Color Doppler US also demonstrated a mass lesion with the pulmonary artery vessel signal sign present (Fig. 6b). Alveolar cell carcinoma was proven by US-guided fine needle aspiration biopsy and surgical resection. This is one of the exceptions in specific consolidation type al-
veolar cell carcinoma with lobar consolidation and a color Doppler US pulmonary artery vessel signal sign present. DISCUSSION Of the imaging examinations (chest radiograph, CT, US, magnetic resonance imaging, angiography and fluoroscopy) used in chest medicine, color Doppler US is the only imaging modality capable of easily and conveniently assessing the vessel signals in peripheral pulmo-
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Fig. 5. (a) Chest radiograph showed fibroproductive infiltrations in the bilateral upper lung fields and active pulmonary tuberculosis was considered. (b) After the chemotherapy for tuberculosis lasting one month, the chest radiograph showed a large mass with cavitation in the left upper lobe. (c) Thoracic CT scan also clearly demonstrated central necrosis in the mass lesion. Clinically, lung cancer was highly suspected. (d) Gray-scale US also revealed a well-defined mass-like lesion at the left upper lobe. (e) However, power Doppler US could easily demonstrate the prominent vessels with the pulmonary artery vessel signal, using waveform analysis. After continuing chemotherapy for tuberculosis for six months, the patient’s condition improved, with only residual lesions on his follow-up chest radiograph.
Color Doppler US pulmonary artery vessel signal ● W.-H. HSU et al.
Fig. 6. (a) Thoracic CT scan revealed consolidation in the left lower lobe with CT-angiogram signs present. (b) Color Doppler US also showed a large mass with color Doppler US pulmonary artery vessel signals. Alveolar cell carcinoma was confirmed by US-guided fine needle aspiration biopsy and surgical resection. This is one exception, in which the color Doppler US pulmonary artery vessel signal was present in specific alveolar cell carcinoma with lobar consolidation.
nary lesions. In our experience, color Doppler US can not only detect the tumor vessel signals in lung cancers, but can also easily predict and confirm pulmonary benign lesions, using the pulmonary artery vessel signal, with high specificity and without any risk (Hsu et al. 1996). Practically, when focusing on the screening for the color Doppler US pulmonary artery vessel signal, the color Doppler US examination is always accomplished within 10 min. This simple technique can eliminate the need for some patients with thoracic lesions mimicking lung cancers (e.g., chronic resolving pneumonia, lung abscesses, fungal infections, tuberculous granulomatous inflammation, organized pneumonia etc.) to undergo immediate semi-invasive or invasive diagnostic procedures, such as thoracoscopic biopsy, surgical resection etc.
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Why did we define the pulsatile flow vessel signal length on sonographic appearance ⱖ1 cm demonstrated by color Doppler US as a pulmonary artery vessel signal? How is the definition of color Doppler US pulmonary artery vessel signal ⱖ0.5 cm or 1.5 cm? As we know, pulmonary benign lesions may have smooth blood supply from both pulmonary arteries and bronchial arteries (Gorg et al. 2003; Hsu et al. 1998, 1996). Although the prominent vessel signals demonstrated by color Doppler US are almost all from pulmonary arteries, a small pulsatile flow with the vessel signal length on sonographic appearance ⱖ0.5 cm demonstrated by color Doppler US may be representative of pulmonary artery or bronchial artery. Thus, the differentiation between pulmonary artery or bronchial artery by using a small pulsatile flow with the vessel signal length ⱖ0.5 cm on sonographic appearance by color Doppler US is somewhat difficult. Why did we not define the vessel signal length ⱖ1.5 cm on sonographic appearance as the color Doppler US pulmonary artery vessel signal? In our series, some benign lesions had the lesion size ⱕ3 cm in diameter, which is often difficult to demonstrate the color Doppler US pulmonary artery vessel signal ⱖ1.5 cm on sonographic appearance (Fig. 2). Practically, color Doppler US pulmonary artery vessel signal ⱖ1.5 cm were always detected in pulmonary lesions ⱖ4 cm in diameter in our series. Based on above findings and our initial experience, we defined the pulsatile flow with the vessel signal length ⱖ1 cm on sonographic appearance demonstrated by color Doppler US as the color Doppler US pulmonary artery vessel signal. In our more than 6 y experience using the color Doppler US pulmonary artery vessel signal to predict the benign lesions, there has been only one exception (as shown in Fig. 6) in which alveolar cell carcinoma presenting as pulmonary lobar consolidation had a pulmonary artery vessel signal. Alveolar cell carcinoma may have the specific CT angiogram sign, which is thought to be due to pulmonary arteries running through the cancer and is specific among the lung cancers presenting with pulmonary consolidations (IM et al. 1990). Clinically, among 125 lung cancers, we have indeed encountered two patients with alveolar cell carcinoma with lobar consolidation presenting with a color Doppler US pulmonary artery vessel signal. Nevertheless, for an experienced physician with expertise in chest US, gray-scale US can easily diagnose alveolar cell carcinoma with lobar consolidation as lung cancer, using the image alone. In addition to lung cancer, we have performed color Doppler US examinations with nine other pulmonary malignancies, including two malignant lymphoma and seven metastatic lung cancers [cervical cancer (n ⫽ 2), endometrial cancer (n ⫽ 1), transitional cell carcinoma of the bladder (n ⫽ 1), colon cancer (n ⫽ 1), nasopharyngeal cancer (n ⫽ 1) and osteogenic sarcoma of the left
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femur (n ⫽ 1)]. Of these, five had detectable color Doppler US pulsatile flow vessel signals [cervical cancer (n ⫽ 1), endometrial cancer (n ⫽ 1), transitional cell carcinoma of bladder (n ⫽ 1), nasopharyngeal cancer (n ⫽ 1) and malignant lymphoma (n ⫽ 1)], but still had no color Doppler US pulmonary artery vessel signal present. Although we had short experience and did not perform pulmonary and bronchial angiograms for metastatic lung cancers, we believe that the color Doppler US pulmonary artery vessel signal could also be used with pulmonary benign lesions to exclude the possibility of metastatic lung cancers. Undoubtedly, the application of the color Doppler US pulmonary artery vessel signal to exclude other pulmonary malignancies warrants a further largerscale study in the future. In other congenital or chronic infectious lung diseases, such as bronchiectasis with organizing pneumonia, pulmonary sequestration, congenital cystic adenomatoid malformation etc., the color Doppler US pulmonary artery vessel signal is often present. However, the detected and prominent pulsatile flow vessel signals may originate from the systemic arteries, not from the pulmonary arteries; in this situation, as shown in Table 1, we called these vessel signals pseudo-pulmonary artery vessel signals (Hernanz-Schulman et al. 1991). Nevertheless, both the color Doppler US pulmonary artery vessel signal and the pseudo-pulmonary artery vessel signal still imply that the pulmonary lesions are benign. Certainly, color Doppler US has some limitations and influencing factors in the detection of vessel signals of thoracic lesions, such as the insonating angle, flow velocity, US probe, anatomic narrowing interface and the necessity for the patient’s cooperation. Moreover, only abutting chest wall lesions can possibly be examined by color Doppler US. Of these, the limitation of detecting slow flow vessels and the influence of the insonating angle are the main concerns of conventional color Doppler US. Nevertheless, there is no doubt that prominent vessels can be easily detected by conventional color Doppler US. Regarding the detection of low-flow vessel signals and the influence of the insonating angle (the Doppler angle : between the ultrasound beam and the flow vessel signals), high-end advanced US equipment and functions have overcome some these limitations (Bude et al. 1994; Rubin et al. 1994). Thus, we believe that rapid improvements in ultrasound equipment and advances in biological technology will broaden the clinical application of color Doppler US. As shown in Fig. 5, we believe the added application of power Doppler US will also significantly increase the sensitivity of color Doppler US to detect the pulmonary artery vessel signal (Bude et al. 1994; Rubin et al. 1994). In conclusion, color Doppler US is helpful in assessing vessel signals in thoracic lesions and the appli-
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cation of the color Doppler US pulmonary artery vessel signal sign is valuable in predicting and differentiating pulmonary benign lesions from lung cancers, with high specificity and without any risk. It is worthy of being widely used in chest medicine, especially with thoracic lesions mimicking lung cancers and without a conclusive diagnosis by conventional examinations. Moreover, it is usually accomplished within 10 min and can lead to the avoidance of some unnecessary semiinvasive or invasive diagnostic procedures. Acknowledgements—This study was supported in part by research grant 13401 from Department of Health, Executive Yuan, Taiwan.
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