Role of Transthoracic Ultrasound in Detection of Pneumonia in ICU Patients

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1 Med. J. Cairo Univ., Vol. 83, No. 1, June: , Role of Transthoracic Ultrasound in Detection of Pneumonia in ICU Patients FARES AUF, M.D.; AHMED ABO-NAGLH, M.D.; MOUSTAFA ZEDAN, M.D. and MOHAMMAD AL-SOKROMI, M.Sc. The Department of Chest, Faculty of Medicine, Al-Azhar Univerisity Abstract Background: X-ray is widely recognized as a crucial step in the diagnosis of pneumonia. The limitations of chest X- ray in the diagnosis of pneumonia are more evident in some sites of care such as the ICU or emergency department. Aim of the Work: The aim of this work is to study the role of transthoracic ultrasound in diagnosis and follow-up of pneumonia in ICU patients. Subjects and Methods: This study was conducted on 38 RICU patients in Bab El-Sha'eria University Hospital suspected of pneumonia by history and physical examination, after recording a written consent at the period from November 2013 to May All patients undergone: Complete history taking, general and local chest examination, laboratory investigation including. CBC, ESR, renal and hepatic profile, CURB-65 score assessment, plain chest radiography, Computerized tomography (CT) chest scan and transthoracic ultrasound was done for all patients. On clinical suspicion of pneumonia, transthoracic ultrasonography was done, then chest radiography was carried out and CT chest was done for all patients (38 patients) as a gold standard test. Then patients was classified into two groups: Confirmed pneumonia group, patients with positive CT finding for pneumonia (30 patients) and confirmed non pneumonia group, patients with negative CT findings for pneumonia (8 patients with other diagnosis). Results: The sensitivity and specificity of transthoracic ultrasound in diagnosing pneumonia in ICU when compared with CT chest were 93.33% and 75.0% respectively. While the sensitivity and specificity of chest X-ray in diagnosing pneumonia in ICU when compared with CT chest were.0% and 62.5% respectively. Conclusion: Transthoracic ultrasound has a valuable role in the diagnosis and follow-up of pneumonia in ICU patients, as it is a bedside real-time, reliable, rapid and noninvasive technique. Recommendation: Pneumonia in ICU could be diagnosed and followed-up by transthoracic ultrasound. Key Words: Pneumonia ICU patients Transthoracic Ultrasound. Correspondence to: Dr. Fares Auf, The Department of Chest, Faculty of Medicine, Al-Azhar Univerisity Introduction PNEUMONIA in adults is a common disorder, potentially life threatening with a high hospitalization rate. Therefore, a correct and rapid diagnosis is mandatory [1]. X-ray is widely recognized as a crucial step in the diagnosis of pneumonia. The limitations of chest X-ray in the diagnosis of pneumonia are more evident in some sites of care such as the ICU or emergency department [2]. Diagnosis of pneumonia by chest CT has became more common, although CT could be considered the "gold standard" technique in the diagnosis of pneumonia, it cannot be used as a firstline radiological examination in all patients with suspected pneumonia, this is mainly due to the fact that it is often not available and that it involves a high radiation dose and is costly [3]. Aim of the work: The aim of this work is to study the role of transthoracic ultrasound in diagnosis and followup of pneumonia in ICU patients. Subjects and Methods This study was conducted on 38 RICU patients in Bab El-Sha'eria Al-Azhar University Hospital suspected of pneumonia by history and physical examination, after recording a written consent, at the period from November 2013 to May All patients underwent: Complete history taking, thorough general and local chest examination, laboratory investigation including. CBC, ESR, renal and hepatic profile, CURB-65 score assessment, plain chest radiography, computerized tomography (CT) chest scan, and transthoracic ultrasound were done for all patients. 307

2 308 Role of Transthoracic Ultrasound in Detection of Pneumonia in ICU Patients Criteria for pneumonia diagnosis: Suggestive history (fever, cough, sputum production, dyspnea). General and local physical signs suggestive of pneumonia [4]. Criteria for I. C. U admission: CURB-65 score 3. The score is an acronym for each of the risk factors measured. Each risk factor scores one point, for a maximum score of 5 [2]. Confusion of new onset. Urea greater than 7mmol/l (19mg/dL). Respiratory rate of 30 breaths per minute or greater. Blood pressure less than 90mmHg systolic or 60mmHg diastolic. Age 65 or older. Exclusion criteria: Pregnant women was excluded because of the restrictions in the use of CT chest which is required for the study. On clinical suspicion of pneumonia, transthoracic ultrasound was done, then chest radiography was carried out. CT chest was done for all patients (38 patients) as a gold standard test. Then patients was classified into two groups Confirmed pneumonia group, patients with positive CT finding for pneumonia (30 patients), and Confirmed non pneumonia group, patients with negative CT findings for pneumonia (8 patients) with other diagnosis. Transthoracic ultrasound: The process was performed by a single physician who was non blinded to patients clinical condition. The ultrasound examination involved longitudinal and oblique scans of the of the anterior, lateral and posterior chest wall. The probe was set perpendicular, oblique, and parallel to the ribs. For a total of 12 areas bilaterally (6 zones per hemithorax). Sonography was performed with a 3-to 6MHz convex transducer because of its suitability to the intercostal approach named (Sonoescape B5). Diagnostic criteria of pneumonia by transthoracic ultrasound: The main diagnostic sonomorphologic criteria of pneumonia by transthoracic ultrasound are defined as follow: Consolidation which is mainly subpleural lung consolidation (presenting a tissular pattern), air bronchograms (impresses a multiple small air inlets within a consolidation measuring a few millimeters in diameter or as a tree shaped echogenic structure) with or without pleural effusion (demonstrated as an echo-poor/echo-free space between visceral and parietal pleura) [5]. Diagnostic criteria of pneumonia by C-T chest: By presence of consolidation and air bronchogram. Plain chest X-ray, was performed either as a supine or seated anterior-posterior view or an upright posterior-anterior views depending on the patient's condition. Diagnostic criteria of pneumonia by X-ray chest: By presence of consolidation, opacity and airbronchogram with or without pleural effusion. The results of transthoracic ultrasound and chest X-ray were compared with chest CT as, a gold standard for pneumonia diagnosis. 38 patient diagnosed as pneumonia on clinical basis X-ray chest, transthoracic ultrasound, C-T chest According to result of C-T chest 30 patient C-T positive for presence of pneumonia (confirmed pneumonia) Criteria for pneumonia diagnosis: Suggestive history (fever, cough, sputum production, dyspnea). General and local physical signs suggestive of pneumonia. Criteria for I. C. U admission: CURB-65 score 3. 8 patient C-T negative for presence of pneumonia (confirmed non pneumonia) other diseases on C-T chest Fig. (1): Flow chart for protocol of research. Results Table (1): Age distribution among the studied groups. Range Mean ± SD ± Table (2): Sex distribution among the studied groups. Sex Confirmed pneumonia Group A (n=30) Chi-Square N % X2 p-value Male Female Total %

3 Fares Auf, et al Male Female Histogram (1): Sex distribution among the studied groups. Table (3): Co-morbidity distribution among the studied groups. Co-morbidity Group A (n=30) N % X2 Chi-Square p-value Chronic Chest Disease DM IHD Renal disease No Co-morbidity Total Table (5): Sensitivity and specificity of CXR in relation to CT chest in the diagnosis of pneumonia in ICU. CXR +ve (succeded) ve (failed) 20% failed Cases by CT chest Confirmed pneumonia N % Total Chi-Square X2 p-value Accuracy * Sens. Spec. PPV NPV Relation of X-ray chest to C-T chest in diagnosis of pneumonia in ICU % succeded Table (4): Sensitivity and specificity of thoracic ultrasound in relation to CT chest in the diagnosis of pneumonia in ICU. U/S +ve (succeded) ve (failed) 7% failed 93% succeded +Ve Cases by CT chest Confirmed pneumonia N % 28 2 Ve Total Chi-Square Sens. X2 p-value Accuracy Spec. <0.001* PPV NPV Relation of thoracic ultrasound to C-T chest in diagnosis of pneumonia in ICU Histogram (2): Relation of thoracic ultrasound to C-T chest in diagnosis of pneumonia in ICU Succeded Failed Histogram (3): Relation of x-ray chest to C-T chest in diagnosis of pneumonia in ICU. Sensitivity and specifcity of chest X-ray and thoracic ultrasound in dianosis of pneumonia in ICU Sens. Chest X-ray 62.5 Spec. 75 Thoracic ultrasound Histogram (4): Sensitivity and specificityof chest X-ray and thoracic ultrasound in diagnosis of pneumonia in ICU.

4 310 Role of Transthoracic Ultrasound in Detection of Pneumonia in ICU Patients Accuracy of thoracic ultrasound and chest X-ray in diagnosis of pneumonia in ICU Accuracy of thoracic ultrasound Accuracy chest X-ray Histogram (5): Accuracy of thoracic ultrasound and chest X- ray in diagnosis of pneumonia in ICU Chest X-ray Thoracic ultrasound % % after 1 week after 2 week Histogram (6): Detection of improvement by CXR and Sonar after 1 week and 2 weeks. Table (6): Sonographic findings in cases of pneumonia. Diagnostic signs N % Total Air bronchogram 18* Consolidation 23* 76.6 Pleural effusion 5* 16.6 Normal findings * Some cases presented by more than one finding. Table (7): Detection of improvement by CXR after 1 week and 2 weeks. Fig. (2-A): X-ray chest with left lower lobe pneumonia. Comparison of detection of improvement* After 1 week After 2 week N % N % CXR: Positive cases at start Not improved Improved Negative cases at start Total cases: X p Table (8): Detection of improvement by thoracic ultrasound U/S after 1 week and 2 weeks. Fig. (2-B): C-T chest of the same patient. Comparison of detection of improvement* After 1 week After 2 week N % N % Thoracic U/S: Positive cases at start Not improved Improved Negative cases at start Total: X p * Improvement appeared by follow-up for number and size of infiltrate by reduction in number and size or by disappearance of infiltrate. Fig. (2-C): Thoracic ultrasound.

5 Fares Auf, et al. 311 Fig. (3-A): Female patient 45 with X-ray shows right lower lobe pneumonia. Fig. (3-B): C-T chest. Fig. (3-C): Thoracic ultrasound. Discussion Transthoracic ultrasound has only recently been appreciated by the greater medical community because for a long time respected sources considered ultrasound to be unfit for assessing the pulmonary parenchyma [6]. On the contrary, during the past decade, lung ultrasound has been shown to be a very useful tool in the hands of intensivists and emergency physicians for the diagnosis of pneumothorax, pleural effusions and other thoracic conditions. Its use in the diagnosis of pneumonia has also been investi- gated in consideration of the great limitations of CXR [7]. This is of particular importance when chest X- ray is performed in the ED, where many patients are critically ill and can be examined only in the supine position, often with bedside equipment [8]. Although chest X-ray is widely recognized as a crucial step in the diagnosis of pneumonia, this technique has several limitations and is not 100% sensitive or 100% specific [9]. During the last decade, diagnosis of pneumonia by chest CT has become more common. Although CT could be considered the "gold standard" technique in the diagnosis of pneumonia, it cannot be used as a first-line radiologic examination in all patients with suspected pneumonia [10]. Thus in the present study we evaluate effectiveness of transthoracic ultrasound to confirm clinical suspicion of pneumonia in ICU patients. In the present study most cases were old age ranged from 43 years to 87 years with mean age ± years. This can be explained by pneumonia in old age is mostly severe (Table 1). This is in agreement with Parlamento et al., study who mentioned that the mean age of confirmed patients with pneumonia was 60.9 years (SD, 21.8) [11]. This result also, is in agreement with Nafae et al., who reported that, the age of 76.25% of confirmed cases with pneumonia was 50 years [12]. In the present study we found that there is a male predominance among the studied groups of pneumonia patients (Table 2). This result is in agreement with Cortellaro et al., study. They found that out of 120 patients with pneumonia 77 were males with a percentage of (64%) [13]. This result also, is in agreement with Nafae et al., who reported that, there were male predominance, as there was 45 male patients of overall patients confirmed as a pneumonia patients with percentage of 56% [12]. In the present study we found that co-morbidities are highly present among studied patients especially, chronic chest diseases in 10 cases (33.3%), and diabetes mellitus in 6 cases (20%) (Table 3). These results are in agreement with Reissig and Kroegel, study who mentioned that in 21 (70%)

6 312 Role of Transthoracic Ultrasound in Detection of Pneumonia in ICU Patients of the patients, pneumonia was associated with co morbidity, mostly with chronic obstructive pulmonary disease (n= 16) [14]. These results also, are in agreement to Nafae et al., study who stated that co-morbidities are highly presented among studied groups of pneumonia patients especially Chronic chest disease and Cardiac disease with percentage of 37% and 31.25% respectively [12]. In the present study we found that cases confirmed to have pneumonia by CT-chest were 30, and cases proved by thoracic ultrasound were 28 cases (succeded) with percentage of success 93.3% in diagnosis of pneumonia in ICU from 30 cases with p-value < and Sensitivity 93,3% and specificity 75% and accuracy (Table 4). In the present study we found that cases proved pneumonia by X-ray chest in relation 30 cases diagnosed by C-T chest were 24 cases with percentage of success % and Sensitivity % and specificity 62.5 for chest X-ray in relation to CT chest in the diagnosis of pneumonia in ICU. With accuracy with p-value This can be explained by the limitation of X- ray in the diagnosis of pneumonia in ICU and emergency settings due to improper positioning of these critically ill patients. In those patients, plain X-ray films are antero-posterior and patients are usually supine. In the present study there were 2 false negative (6.6%) failed to be diagnosed by thoracic ultrasound, that is due to limitation of the lung ultrasound to detect deep lung lesions (Table 4). This is in agreement with Bourcier et al., 2007 study they found there were 6 false negative results observed by lung ultrasound from 144 patients involved in the study (4. 1 %). They reported that ultrasound performance is probably very good at detecting superficial pneumonia, it remains however poor at detecting deep alveolar lesions [15]. These results also, in agreement with Reissig and Copetti, study who reported that there were about 8% of patients diagnosed as pneumonia patients could not be detected by Lung ultrasound, because ultrasound may only detect lesions reaching the pleura [16]. In the present study, echographic findings in cases of pneumonia were consolidation in 23 cases (76.6%), air-bronchogram sign in 18 cases (60.00%), pleural effusion in 5 cases (16.6%), and most of the cases have more than one finding (26 cases with percentage of 86.6%) (Table 6). These results are in contrast with Reissig and Kroegel, study who found that multiple hyperechoic inclusions indicating air inlets within the pneumonic lesions (positive bronchoaerogram) were shown in 32 of 33 (96.9%) pneumonias. Intense bronchoaerograms were visible in 3 of the 32 cases (9.3%), whereas the bronchoaerogram in 6 patients was weak (i.e. only few hyperechoic inclusions were found). No bronchoaerogram could be detected in only 1 patient (3%). They concluded that thoracic ultrasound represents a further imaging technique for identifying pneumonic lesions and thus provides an additional tool for diagnosing pneumonia [14]. Cortellaro et al., study found that: Pattern of consolidation in 73 from cases (91.25%) with dynamic air bronchograms almost always present within the consolidation. An interstitial pattern surrounded the consolidation in 42 cases from cases (52.5%) as an expression of perilesional inflammatory edema [13]. These results agreed with Reissig and Kroegel, 2007 study who found that the sensitivity and specificity of thoracic ultrasound in diagnosing pneumonia were 93.4% and 97.7% [14]. These results, also are in agreement with Cortellaro et al., study that ultrasound showed a sensitivity of 99% and a specificity of 95%, Chest X- ray fared much worse, with a sensitivity of 67% and a specificity of 85% [13]. This study also, agreed with Nafae et al., who found the sensitivity and specificity of lung ultrasound in diagnosing pneumonia when compared with CT chest were 97.5% and 75.0% respectively and for chest X-ray were 77.5% and 60% [12]. Bourcier et al., also agreed with these results as it found a significantly higher sensitivity of lung ultrasound for the diagnosis of acute pneumonia compared to chest X-ray (95% vs 60%, p<0.0 1). Interestingly lung ultrasound appears to be particularly more effective than chest X-ray when pneumonia is evolving for less than 24 hours [15]. In the present study we found that the cases confirmed not to have pneumonia by CT-chest were 8 cases from 38 cases. These cases presented with clinical suspicion of pneumonia and C-T chest show other diagnosis include two cases with mass lesion with distal Collapse, one case with Subpulmonic empyema, one case with deep seated lung abscess, one case with acute exacerbation for bronchectasis, one case with pulmonary embolism and infarction and two cases with acute exacerbation of COPD with heart failure and right side pleural effusion.

7 Fares Auf, et al. 313 These results are in agreement with Bourcier et al., who reported that: 9 patients who were diagnosed with pneumonia from 144 patients after lung ultrasound had another diagnosis: 4 patients with sepsis of other origin, 2 patients with pulmonary embolism, 1 with acute respiratory distress syndrome, 1 with pulmonary fibrosis and one with acute anemia from gastric origin [15]. These results also, agree with Cortellaro et al., 2012 who mentioned that there were two false positive results. One of the two false-positive patients had a subphrenic abscess with atelectasia of the right lung just above the diaphragm and a small pleural effusion, whereas the other had cardiac failure with pleural effusion and atelectasia [13]. In the present study we found that during follow-up of pulmonary infiltrate in the cases for two weeks by X-ray and thoracic ultrasound, the same course for the pulmonary lesions was present and the detection of improvement (appeared by reduction in number, size or by disappearance of infiltrate) in cases of pneumonia by lung ultrasound more than by chest X-ray. After the first week the detection of improvement by chest X-ray and thoracic ultrasound were 13.3% and 40% respectively, while after the second week the ratios were 66.67% and 86.6% respectively without statistically significant difference (Tables 7,8). These results are in agreement with Angelika and Claus, 2007 they reported that during follow-up of pneumonia in 33 pulmonary infiltrate by using thoracic ultrasound and X-ray for comparison the course of pneumonia they found that, lesions decreased in size or disappeared (30/33) or decreased in number (4/9). The bronchoaerogram became less pronounced (13/32), basal pleural effusion either diminished (7/20) [17]. Conclusion: Transthoracic ultrasound has a valuable role in the diagnosis and follow-up of pneumonia in ICU patients, as it is a bedside realtime, reliable, rapid and noninvasive technique. Recommendation: Pneumonia in ICU could be diagnosed and followed-up by transthoracic ultrasound. References 1- ALMIRALL J. and BOLÍBAR I.: Risk factors for community acquired pneumonia in adults: A population-based case-control study. Eur. Respir. J., 13 (2): , LIM W.S., BAUDOUIN S.V. and GEORGE R.C.: BTS guidelines for the management of community acquired pneumonia in adults: Update Thorax, 64 (Suppl. 3): III 1-55, SYRJALA H., BROAS M., SURAMO I., et al.: Highresolution computed tomography for the diagnosis of community acquired pneumonia. Clin. Infect. Dis., 27: , JONTHAN GLEADLE: History and examination at a glance, pneumonia, Blackwell Science, page 166, SPERANDEO M., CARNEVALE V., MUSCARELLA S., et al.: Clinical application of transthoracic ultrasonography in inpatients with pneumonia. Eur. J. Clin. Invest., 41 (1): 1-7, BECKH S., BOLCSKEI P.L. and LESSNAU K.D.: Real time chest ultrasonography. A comprehensive review for the pulmonologist. Chest, 122: 1759e73, WEINBERGER S.E. and DRAZEN J.M.: Diagnostic procedures in respiratory diseases. Harrison's principles of internal medicine. 17 th edn. New York: McGraw-Hill, Chapter 247, ESAYAG Y., NIKITIN I. and BAR-ZIV J.: Diagnostic value of chest radiographs in bedridden patients suspected of having pneumonia. Am. J. Med., 123: 88.e1e5, ALBAUM M.N., HILL L.C. and MURPHY M.: Interobserver reliability of the chest radiograph in communityacquired pneumonia. PORT Investigators. Chest, 110: , GEHMACHER O., MATHIS G., KOPF A. and SCHEIER M.: Ultrasound imaging of pneumonia. Ultrasound Med. Biol., Vol. 21. No. 9. pp. I I IY 1122, PARLAMENTO S., COPETTI R. and DI BARTOLOMEO S.: Evaluation of lung ultrasound for the diagnosis of pneumonia in the ED. Am. J. Emerg. Med., 27 (4): , NAFAE and SHEBL R. EMAN: Adjuvant role of lung ultrasound in the diagnosis of pneumonia in intensive care unit-patients. Egyptian Journal of Chest Diseases and Tuberculosis, 62: 281-5, CORTELLARO F., COLOMBO S., COEN D., et al.: Lung ultrasound is an accurate diagnostic tool for the diagnosis of pneumonia in the emergency department. Emerg. Med. J., 29: 19-23, REISSIG A. and KROEGEL C.: Sonographic diagnosis and follow-up of pneumonia: A prospective study. Respiration, 74 (5): , BOURCIER J.E., BRICCOLI A., GALLETTI S. and SALONE M.: Ultrasonography is superior to computed tomography and magnetic resonance imaging in determining superficial resection margins of malignant chest wall tumors. J. Ultrasound. Med., 26: , REISSIG A and COPETTI R.: Lung Ultrasound in the Diagnosis and Follow-up of Community-Acquired Pneumonia: A Prospective, Multicenter, Diagnostic Accuracy Study. Chest, Vol. 142, No 4, pp , ANGELIKA REISSIG and L. CLAUS KROEGE: Sonographic diagnosis and follow-up of pneumonia: A prospective study, Respiration, 74: , 2007.

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