Sonographic Approach to Diagnosing Pulmonary Consolidation

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1 Sonographic Approach to Diagnosing Pulmonary Consolidation Remi Targhetta, MD, Roseline Chavagneux, MD, Jean-Marie Bourgeois, MD, Michel Dauzat, MD, Pierre Balmes, MD, Leandre Pourcelot, MD Thirty-nine consecutive patients with consolidated lung confirmed radiologically underwent sonography, and their sonograms were compared with results for 100 healthy subjects. The hyperechoic line of normal aerated lung and its air artifacts showed respiratory motions ( gliding sign/ n = 100). Patients with pneumonia demonstrated distinct sonographic patterns. Strong linear echoes with characteristic air artifacts (air bronchogram) and anechoic tubular structures (fluid bronchogram) were visualized in 36 of 39 patients (92.30%). The superficial lung showed a homogeneous hypoechoic band termed '"superficial fluid alveolo grams (n 39) with respiratory motions in 35 of 39 patients. We conclude that sonography can evaluate pulmonary consolidation and may provide additional roentgenographic information, especially when fluid bran chograms are visualized. KEY WORDS: Ultrasound study; Lung; Pulmonary consolidation; Air bronchogram; Fluid bronchogram; Fluid alveologram. P ulmonary consolidation is frequently seen in daily radiology practice. Because traditionally air has been considered an obstacle to the transmission of ultrasound beam, it would seen inconceivable that a normal aerated lung can be visualized. However, when the alveolar air adjacent to the chest wall is replaced by fluid, the lung disease can be detected ultrasonically. 1 Very few studies have examined the echographic appearance of inflammatory lung diseases. Dome 1 described the sonographic fluid bronchogram in one case of bilateral pneumonia, showing that bronchi containing fluid in consolidated lung can be identified sonographically. Weinberg and coworkers 3 reported the first results in the sonographic diagnosis of pulmonary consolidation, using the air bronchogram sign in 30 pediatric patients. Received April 3, 1992, from the Departments of Internal and Pulmonary Medidne (R. T., P. B.) and Radiology and Ultrasound (R. C, J.-M. B. M. D.), Montpellier-Nimes University Hospital, Nimes, and the Department of Ultrasound (L. P.), Tours University Hospital, Tours, France. Revised manuscript accepted for publication July 9, The purpose of this investigation is to describe the sonographic appearances and evaluate the usefulness of ultrasonography in the diagnosis of pulmonary pa renchymal consolidation, confirmed by chest radio graph in cases without pleural effusion. MATERIALS AND METHODS We conducted a prospective study in 39 adult patients (29 male and 10 female patients) from january 1987 to December 1990 and compared these patients with 100 healthy test subjects. In the control group (72 men, 28 women), the age range was 16 to 66 years with an average age of 41 years. In the consolidated lung group, the age range was IS to 77, with an average age of 46 years. All patients had fever or cough, or both, and radiographic signs of segmental, lobar, or total lung consolidation (n = 39) without pleural effusion visible on standard frontal or lateral radiographs before the sonographic examination. All examinations were performed using a real-time unit (Aloka 250 and 650, Tokyo, japan) with linear or Address correspondence and reprint requests to Remi Targhetta, curved array scanners (3.S MHz and 7.5 MHz). Realtime imaging pictures were recorded on videotapes, MO. Department of Internal and Pulmonary Medicine, Ga5ton Doumergue Hospital. 5, rue Hoche, Nima, 1992 by the American Institute of Ultrasound in Medicine 1 Ultrasound Med 11: , /92/$3.50

2 668 DIAGNOSING PULMONARY CONSOLIDATION 1 Ultrasound Med 11: , 1992 and pictures were taken on x-ray film. Water ~soluble ultrasound transmission gel (Aquasonic, Parker) was applied to the skin as a coupling medium.. The examination consisted of echographic investigation of each hemithorax, with patients seated or supine, with serial recordings of longitudinal (posterior, axillary, and an terior) and oblique or transverse scans, particularly through the intercostal space. The real time observation of the lung surface showed, in all healthy test subjects (n = 100), backand-forth motions synchronous with respiratory movements. The hyperechoic line of pulmonary reflection with a large area of characteristic air artifacts is the only sonographic pattern seen in normal aerated lung. The use of high-frequency probes (7.5 MHz), especially through the intercostal space, avoiding the ribs, facilitates this examination of the pulmonary interface and its respiratory movements, clearly delineated from the soft tissues, termed the Mgliding sign.' 4 However, if the alveolar air adjacent to the chest wall is replaced by f1uid and consequently permits a sonographic acoustic window, consolidated lung could be expected to be visualized by a sonographic examination. This hypothesis was evaluated in 39 adult patients. We particularly studied the strong nonpulsatile linear echoes caused by air-filled bronchi (sono graphic air bronchogram) 3 and the branching, nonpul satile, anechoic tubular structures (sonographic f1uid bronchogram). 2 The echogenidty, the margins, and the respiratory motions of the lesions also were analyzed. RESULTS All patients with radiological lung consolidation had abnormal sonographic findings compared with the control subject images. The results are summarized in Table 1. Echogenicity, Air Bronchogram, Fluid Bronchogram As the echogenicity of the lesions was compared with that of the hyperechoic normal surrounding lung surface, pulmonary consolidation showed heterogeneous (anechoic, hypoechoic and hyperechoic) patterns (Figs. 1 to 3). Strong nonpulsatile linear echoes 3 caused by air filled bronchi (Figs. 1 to 3) were seen in 36 of 39 patients (92.30% ). Anechoic and non pulsatile tubular structures (Figs. 18, 4, 5), a pattern termed the sonographic fluid bronchogram, 2 were demonstrated in 36 of 39 patients (92.30%). The fluid bronchogram diameters at the root of the lung were seen to be decreas ing toward the pulmonary surface (Fig. 4). In one case, diameters increasing toward the periphery were observed. All sonographic patterns (n = 39) of the superficial consolidated lung showed a homogeneous hypoechoic band without air or f1uid bronchograms (Figs. 1-6). We termed this sonographic feature Msuperficial f1uid al veolograms' (Fig. 6). In 3 of 39 patients, only an area of fluid alveologram without bronchogram was ob served (7.69% ). Two patients demonstrated a son'ographic pulmonary consolidation with a central anechoic area, not suggested by chest radiograph. Anterior and Posterior Margins The sonographic interruption of highly reflective pleuropulmonary surface echoes (Figs. 2, 3) was found in all patients. The posterior margins (Fig. 2 to 4) were Table 1: Sonographic Findings in Patients with Consolidated Lung (n 39), Including 3 Patients with Isolated MSuperficial Fluid Alveolograms' Sonographic Findings Consolidated Lung Number(%) Echogenicity Heterogeneous 36 (92.3%) Homogeneous and hypo 3 (7.6%) echoic Air bronchogram Hyperechoic linear echoes 36 (92.3%) with air artifacts Fluid bronchogram Anechoic tubular structure 36 (92.3%) Superficial margin Interruption of hyper 39 (100%) echoic lung surface Posterior margin Irregular 37 (94.8%) Regular 2 (5.1%) Increase in artifactst 39 (100%) Respiratory motion Present 35 (89.7%) No diaphragmatic excur- 4 (10.2%) sian Homogeneous and hypoe<:hoit superficial nuid alveolograms isolated in three cases or pulmonary consolidation. t Increase in characteristic air artiract ~ deep to the lesion.

3 JUltrasound Med 11: , 1992 TARGHETTA ET AL 669 Figure 2 Middle lobe pulmonary consolidation (anterior and posterior margins; intercostal sonogram 3.5 MHz). The interruption (1) of hyperechoic (2) lung surface, permitting a sonographic superficial fluid alveologram window with no tapered left edge, is clearly visualized. The posterior margins (3), with an increase of the hyperechoic artifacts (4), are irregular. Sonographic fluid (5) and air (6) bronchograms can be discerned. In real-time images, respiratory motions of the lung consolidation could be demonstrated. irregular 94.87%) in all but two patients. An increase of hyperechoic artifacts mimicking enhancement, deep to the lesion (Figs. 2 to 4), was observed in all cases. When the scanning was done with different angles at the boundary of the lesion, sonograms revealed at least one side with no tapered edge in each patient (Figs. 2, A 3). Respiratory Motions On real-time images, respiratory motions of the pulmonary consolidation could be demonstrated clearly in Figure 3 Heterogeneous echogenicity caused by sonoa graphic air and fluid bronchograms (intercostal sonogram 3.5 MHz). Air bronchograms (1) and fluid bronchograms (2) are seen in consolidated lung. Note the sonographic interruption (3) of the aerated (4) hyperechoic pulmonary surface. 8 Figure 1 A, CT scan in a patient with right lower lobe pneumococcal pneumonia. 8, Sonographic lung consolidaw tion through the 8th right intercostal space, same patient (air and fluid bronchograms). This sonogram, using 3.5 MHz scanner, reveals sonographic air bronchograms (1) with pos~ terior air artifacts. Note the anechoic tubular branching struc+ tures termed sonographic fluid bronchograms in transverse (2) and longitudinal views (3), not visualized in A. (4), Soft tissues of the chest wall. Superficial fluid alveolograms are seen (arrows).

4 670 DIAGNOSING PULMONARY CONSOLIDATION Figure 4 Sonographic fluid bronchograms (transverse sec~ tion, 3.5 MHz). The diameters of fluid bronchograms (1) at the root of the lung were seen to decrease toward the pulmonary surface (2). Those bronchograms let the sound waves in and are characterized by an anechoic tubular structure without shadowing deep to the bronchi. Note that the transverse sections of linear fluid bronchograms are more or less linear depending on the quality of the lateral resolution of the scanner, which is known to deteriorate with depth. Rib (3) and its acoustic shadow are seen, as is the chest wall (4). 35 of the 39 patients (89.74%). In the four other cases, diaphragmatic excursion was not observed, explaining the loss of the "gliding sign in pneumonia. DISCUSSION On the basis of this prospective study of pulmonary consolidation, which was confirmed radiologically, we Figure 5 Sonographic fluid bronchograms (longitudinal section, 3.5 MHz). Sonogram enlargement showing an ane~ choic, nonpulsatile, branching tubular structure (1) sur rounded by fluid alveolograms (2) and air bronchograms identified by the posterior comet-tails (3). J Ultrasound Med 11: , 1992 Figure 6 Sonographic superficial fluid alveolograms (in tercostal sonogram 7.5 MHz), (1) caused by air adjacent to the chest wall replaced by fluid in alveolar spaces, are identified sonographically as hypoechogenic homogeneous areas. By using 7.5 MHz scanner in the intercostal space and avoid ing the ribs, echography can clearly visualize air broncho grams (2) and the respiratory motions of the pulmonary surface (3), well-delineated from the soft tissues of the chest wall (4). The measured distances of the superficial fluid alveolograms from the lung surface (3) to the bronchograms (2) are between 9 and 11 mm. have been able to identify the sonographic features of inflammatory lung diseases. We compared the abnormal so'\ograms with those of 100 control subjects. In our series of 39 patients, in every case in which consolidation was present on chest film, the sonogram demonstrated abnormalities. Sonographic air bronchograms (92.30%), fluid bronchograms (92.30%), and superficial fluid alveolograms (100%) can be observed. Air has traditionally been said to totally reflect sound waves, which probably accounts for the paucity of publications about the sonographic aspects of pulmonary consolidation. In 1986, Oome2 reported the sonagraphic fluid bronchogram sign in one patient with a bilateral pulmonary consolidation. The ability to differentiate consolidated lung from pleural disease using the fluid bronchogram was demonstrated. Neither the chest radiograph nor the thoracic CT scan without intravenous contrast material, in this case, could distinguish pleural collection from pneumonia. Bronchi con taining fluid can be visualized via ultrasonography as branching, nonpulsatile, and anechoic tubular struc~ tures.2 Soon after Dome's report appeared, Weinberg and colleagues::! described a new sonographic pattern in 30 pediatric patients with clinical and radiographic evidence of pneumonia. The sonographic air bronchogram produced nonpulsatile linear, high-amplitude branching echoes with posterior characteristic air artifacts,~ caused by air filled bronchi. However, the au-

5 J Ultrasound Med 11: , 1992 thors did not mention the visualization of the fluid bronchogram. In healthy subjects, because air totally reflects sound waves, the pleuropulmonary surface appears as a highly echogenic line, generating a large area of echo artifacts. 6 Normal aerated pulmonary parenchyma, deep to the lung surface, cannot be analyzed using ultrasonography. In such subjects, observation of the hyperechoic line in real time reveals back~and forth movements synchronous with respiration. We termed this motion the gliding sign/ 4 which should always be looked for in thoracic sonography.7 The disappear ance of diaphragmatic excursion was clearly diagnosed by real-time sonographic examination, and conse quently the absence of the gliding sign of pulmonary consolidation (in 4 of 39) may be interpreted as possible phrenic paralysis caused by inflammatory lung disease. The sonographic bronchograms cannot be obtained in normal subjects because air totally reflects sound waves. However, when the aerated lung adjacent to the chest wall is replaced by fluid, pulmonary consolidation becomes detectable sonographically. Some pulmonary infiltrates could theoretically not be visualized by sonography- e.g., medial segment of the middle lobe, if the aerated lung lies between the chest wall and the region involved by pneumonia. Nevertheless, in our series of 39 patients, we found, in each patient with acute pneumonia, an acoustic window to delineate echo patterns of pulmonary consolidation. At the very least, sonography reveals only superficial fluid alveolograms (3 of 39); fluid- or air-filled bronchi can be identified if no aerated pulmonary parenchyma lies between the chest wall and the bronchi. Sonographic patterns easily distinguish air from fluid bronchograms. An air bronchogram, reflecting ultrasound beams totally, appears as a hyperechoic line with posterior artifacts. 5 On the other hand, the fluid bronchogram lets the sound waves in and is characterized by an anechoic tubular structure without shadowing deep to the lesion. It must be mentioned that chest radiographs cannot detect the fluid bronchogram. The diameter of the bronchi normally decreases toward the superficial fluid alveologram. However, in one case of pneumonia, increasing diameters suggests a consolidated lung with sonographic fluid bronchectasis. In two patients, the central anechoic area in inflammatory lung disease can be interpreted as probably the initial sonographic ap pearance of lung abscess. Sonographic air and fluid bronchograms are probably specific indicators in consolidated lung disease, as are chest radiograph air bronchograms. It appears difficult that ultrasonography without Doppler may distinguish a fluid bronchogram from anechoic vessel in a low-pressure pulmonary system, based on the finding of a nonpulsatile area on real time. However, this theoretical consideration is not important: the sonographic visualization of TARGHETTA ET AL 671 fluid bronchogram or vascular structure implies, in all cases, pulmonary consolidation. 2 The fluid tubular structures could at first sight mimic liver or spleen echoes, especially in pneumonia of the lower lobe. In such cases, sonography clearly identified the inflammatory lesion above the hyperechoic hemidiaphragm, which was easily recognized. Pulmonary ultrasonically guided aspiration biopsy, including of consolidated lung, could be performed in selected patients when the lesion was not diagnosed by such means as sputum examination and techniques using the fiberoptic bronchoscope. Peripheral pulmonary lesions adjacent to the chest wall are more often biopsied under ultrasonographic control. 8 ~ 13 Chandrasekhar and associates first stressed the usefulness of ultrasonography for guiding the percutaneous biopsy of peripheral pulmonary masses. 8 Furthermore, diag nosis of pneumothorax by sonography immediately after a pulmonary ultrasonically guided aspiration biopsy has become possible. 1 ~ The emergence of a gassy pleural effusion was characterized by the sonographic disappearance of the lung lesion. 14 In those cases, sonography proved helpful by visualizing the top of the needle during puncture and after that was employed in the search for a possible pneumothorax. Until recently, ultrasonography has been considered to have limited application in the diagnosis of respiratory disease. Echography offers a new method for the diagnosis of pulmonary consolidation and should be recognized by sonographers. In thoracic disease, radiographs remain indispensa ble. However, we believe that ultrasonography may provide complementary noninvasive findings and could be particularly helpful in the evaluation of com plex pleuroparenchymal disease. When fluid-filled bronchi are visualized, sonographic examination can add important information, if necessary, in interpreting chest radiographs. In addition to its simplicity, porta bility, and lack of need for ionizing radiation, echog raphy can also be particularly useful for emergency situations if no radiologic equipment is available. However, the number of patients in our study was limited, and definite conclusions should await further prospective investigations. REFERENCES 1. Hendin A: Ultrasonic pulmonary densitometry: Prelimi nary studies. Invest Radiol10:258, Dome HL: Differentiation of pulmonary parenchymal consolidation from pleural disease using the sonographic fluid bronchogram. Radiology 158:41, Weinberg B, Diakoumatis EE, Kass EG, et al: The air bronchogram: Sonographic demonstration. 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