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(Chest. 2005;128:1531-1538.)
© 2005 American College of Chest Physicians

Thoracic Ultrasound for Diagnosing Pulmonary Embolism*

A Prospective Multicenter Study of 352 Patients

Gebhard Mathis, MD; Wolfgang Blank, MD; Angelika Reißig, MD; Peter Lechleitner, MD; Joachim Reuß, MD; Andreas Schuler, MD and Sonja Beckh, MD

* From Landeskrankenhaus Hohenems (Dr. Mathis), Klinikum am Steinenberg Reutlingen (Dr. Blank); Pneumologie & Allergologie (Dr. Reißig), Friedrich Schiller Universität Jena; Bezirkskrankenhaus Lienz (Dr. Lechleitner); Kreiskrankenhaus Böblingen (Dr. Reuß); Helfensteinklinik Geislingen (Dr. Schuler); and linikum Nord Nürnberg (Dr. Beckh).

Correspondence to: Gebhard Mathis, MD, Innere Medizin, Landeskrankenhaus Hohenems, Bahnhofstraße 31, A-6845 Hohenems, Austria; e-mail: gebhard.mathis{at}cable.vol.at


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Pulmonary embolism (PE) continues to be a major challenge in terms of diagnosis, as evidenced by the fact that many patients die undiagnosed and/or untreated. The aim of this multicenter study was to determine the accuracy of thorax ultrasound (TUS) in the diagnosis of PE (TUSPE).

Methods: From January 2002 through September 2003, 352 patients with suspected PE were examined in seven clinics. The patients were investigated prospectively by TUS according to the following criteria: (1) PE confirmed: two or more typical triangular or rounded pleural-based lesions; (2) PE probable: one typical lesion with pleural effusion; (3) PE possible: small (< 5 mm) subpleural lesions or a single pleural effusion alone; or (4) normal TUS findings. In all cases, CT pulmonary angiography (CTPA) was used as the reference method. In the event of discrepant findings, a combination of duplex sonography of the leg veins, echocardiography, ventilation/perfusion scintigraphy, and a quantitative enzyme-linked immunosorbent assay or latex d-dimer, or a biopsy/autopsy was performed.

Findings: PE was diagnosed in 194 patients. On TUS, 144 patients had a total of 333 subpleural lesions (mean, 2.3 lesions per patient) averaging 15.5 x 12.4 mm in size. Additionally, a narrow pleural effusion was found in 49% of the patients. TUS yielded the following results under application of the strict criteria 1 and 2: PE true-positive, n = 144; PE false-positive, n = 8; PE true-negative, n = 150; and PE false-negative, n = 50. The sensitivity was 74%, specificity was 95%, positive predictive value was 95%, negative predictive was value 75%, and accuracy was 84%, at a prevalence of 55%. The sensitivity in patients with criterion 1 was 43% and a specificity of 99%.

Interpretation: TUS is a noninvasive method to diagnose peripheral PE. In the absence of CTPA, TUS is a suitable tool to demonstrate a PE at the bedside and in the emergency setting.

Key Words: chest ultrasound • echocardiography • pulmonary embolism • spiral CT • ultrasonography • vein Duplex


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Pulmonary embolism (PE) is a frequently undiagnosed and untreated disease. The incidence of PE in the United States is 23 to 69 per 100,000, and estimated at 10 per 100,000 persons per year.12 The age-adjusted mortality rate due to PE decreased from 19.1 per 100,000 in 1979 to 9.4 per 100,000 in 1998.3 Reducing mortality rates secondary to this insidious disease is a challenge and justifies the application of all available diagnostic procedures.4

"Nonspecific" clinical symptoms are the main problem; they rarely cause the physician to suspect a PE. The Prospective Investigation of Pulmonary Embolism Diagnosis study5 showed that ventilation/perfusion (/) scintigraphy is not sufficiently conclusive for making the diagnosis. In the last decade, CT pulmonary angiography (CTPA) has been established as the method of choice for the diagnosis of central PE up to the level of the segmental arteries, as it is able to show the thromboembolic obstruction directly.67 However, single-slice CTPA is of limited value in subsegmental arteries.89 In recent years, several efforts have been made to improve the diagnosis by the use of multislice CTPA and magnetic resonance tomography. Multislice CTPA at thin collimation significantly improves the visualization of segmental and subsegmental arteries and reduces respiration and cardiac motion artifacts.101112 However, the application of this procedure failed in many instances because of the time factor and the nonavailability of the imaging equipment. Patients with unstable hemodynamics cannot easily be transported.13 Eventually, a number of examinations became part of the clinical algorithm to be applied in daily clinical practice, namely the d-dimer test, CTPA, (/) scintigraphy, echocardiography, and leg vein duplex sonography. These procedures constitute a diagnostic mosaic that is hoped to yield more or less accurate results.

In the late 1960s, a number of investigators141516 pointed out that a large number of peripheral lung lesions caused by PE could be shown on A scan, compound scan, and B scan sonography. For 10 years, we have been familiar with the sonomorphology of PE on the B-mode sonographic image.17 The accuracy of chest ultrasound in the diagnosis of PE has been described in several studies.18192021

The aim of the present prospective, multicenter study was to determine the value of thorax ultrasound (TUS) in the diagnosis of PE (TUSPE). The examinations were conducted by investigators with varying degrees of experience, around the clock, in a hospital-based medical care setting.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Setting
Seven institutions participated in the study: one department of pneumology in a medical university clinic, and another pneumology center; two medical clinics specialized in gastroenterology; and three departments of general internal medicine with affiliated coronary care units. Most patients were sent to these institutions either by general practitioners or by specialists.

The institutions participating in the study had the necessary equipment, competence, and manpower for ultrasound investigation: abdominal, chest, echocardiography, and vascular. The occasional nonavailability of a competent investigator was a limiting factor in some instances because, in addition to their own ward, the investigators were called to the emergency department and also served as consultants for other wards in the hospital.

Chronic and specific lung diseases were treated in pulmology departments. Patients with risk factors such as cancer or immobility were seen in gastroenterology departments, while a broad spectrum of diseases including PE were seen in the general internal medicine department. Thus, PE was encountered regularly, but not very frequently, in these institutions. Major limiting factors in some centers were manpower and the availability of an investigator. However, this fact was not considered to influence the results to a significant extent.

Patient Selection
In the present study, the main criterion for acceptance was clinical suspicion of PE under consideration of the risk factors. Symptoms and risk factors were documented. As every clinical suspicion of PE had to be confirmed, the patients were not stratified into different pretest probabilities. Patients with deep vein thrombosis without symptoms of PE were excluded. Three groups of patients were included in this study: (1) outpatients who came to the outpatient department of the hospital on their own (3%); (2) patients with suspected PE, sent to the hospital by external medical institutions (54%); and (3) patients in whom PE was identified or suspected during their inpatient stay (43%).

Due to the nature of the referral pattern, our centers were more often in the situation to confirm rather than exclude PE, as it is often the case in radiology centers. This might explain the high prevalence of pulmonary embolism in our centers. Informed consent was obtained from all patients. The trial protocol was approved by the local ethics committee.

Final Diagnosis of PE
Single-slice CTPA was used as the reference method. The CT examinations were performed at the local radiology institute. A radiologist interpretation of the digital images, based on standard guidelines, was included in the protocol. The scans were not reviewed a second time.

CT is not a standard procedure to investigate subpleural lesions in PE. This was taken into account for the final diagnosis, as discussed in the published literature. At the radiology institutes involved in the present study, subpleural findings were recorded, localized, and measured beyond the confines of clinical routine because one aim of the study was to compare CTPA and TUS with regard to the size of subpleural lesions.

In the event of a negative CTPA result, the usual clinical algorithm was used. At least two of the following criteria had to be positive for the final conclusive diagnosis of PE: (1) high clinical suspicion; (2) positive d-dimer finding in outpatients; (3) proven leg vein thrombosis on duplex sonography; (4) characteristic grade 3 or 4 changes on echocardiography; (5) a high-probability / scan; (6) angiography of the pulmonary artery; (7) biopsy/necropsy.

In order to reduce the time factor of thrombolysis, a CTPA within 24 h was mandatory when PE was suspected. Echocardiography within 24 h was obligatory in cases of grade 3 or grade 4. Duplex sonography of the leg veins was conducted during the same session if possible, at the latest within 5 days.

Plasma d-dimer levels were measured using an interleukin d-dimer latex test or a usual quantitative enzyme-linked immunosorbent assay. Follow-up investigations were performed during the hospital stay.

Thoracic Ultrasound
In cases of a clinically suspected PE, a chest sonography was performed prior to other imaging procedures. The sonogram was obtained, whenever possible, with the patient in a sitting position. The patient raises his or her arms and places their hands at the back of the head in order to slightly extend the intercostal spaces and rotate the scapula outward. The surface of the lung was scrutinized for subpleural lesions on standardized longitudinal sections and along the intercostal spaces. Either a curved array or a sector scanner (3.5 to 6 MHz) was used for sonographic examination. The investigator had to have conducted at least 100 chest sonograms previously. The examinations were performed around the clock. The following criteria were used for the ultrasound diagnosis: (1) PE was considered when two or more characteristic triangular or rounded pleura-based lesions were demonstrated; (2) PE probable: one typical lesion with a corresponding low-grade pleural effusion; (3) PE possible: nonspecific subpleural lesions < 5 mm in size or a single pleural effusion alone; and (4) PE not established: normal chest sonography. The following was determined on the basis of TUS: location, number, size and form of the lesions, and the presence of a local or basal pleural effusion.

Statistical Analysis
Baseline characteristics between diagnostic groups were compared using the {chi}2 test or Mann-Whitney U test as appropriate. Wilcoxon signed-rank test and Spearman correlation coefficient were used to assess differences and associations of quantitative measures. To compare diagnostic accuracy, the 95% confidence intervals for prevalence, sensitivities, specificities, and positive and negative predictive values were determined; p < 0.05 was considered to indicate statistical significance (StatXact 4.0; Statistical Solutions; Saugus, MA).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patients
We included 352 patients with clinically suspected PE in the multicenter trial. Of these, 194 patients (55%) had a final diagnosis of a PE. Patient data are listed in Table 1 .


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  		Table 1.. Data From 352 Patients Suspected of Having PE

 
During the study period, PE was established at the time of discharge in 393 cases. The final diagnoses were registered in the central account system of the hospitals. Of those patients with PE at the time of discharge, 199 patients (51%) could not be included in the study. A projected number of 710 patients were suspected of having a PE. The factors the limited the inclusion of patients into the study were estimated. These included the following: (1) the patient was in the ICU and could not be transported; the diagnosis was mainly established by echocardiography (11%); (2) CTPA could not be performed because of a contrast agent allergy or renal failure, or was not available in the time window (33%); (3) TUS could not be performed because of the unavailability of a trained ultrasound physician (33%); the diagnosis was mainly established by / scintigraphy (3%); (5) the patients did not fulfill other inclusion criteria (20%).

The final diagnosis was confirmed by CTPA in 169 patients (87%). In a further 25 patients, suspected PE was confirmed by the following clinical algorithms: d-dimer test (n = 23), leg vein duplex sonography (n = 14), echocardiography (n = 5), and / scintigraphy (n = 2).

TUS Results
TUS yielded the following results under application of the strict criteria 1 and 2: sensitivity, 74%; specificity, 95%; positive predictive value, 95%; negative predictive value, 75%; accuracy, 84%; at a prevalence of 55% (Fig 1 ; Tables 2, 3 ). The different categories (confirmed, probable, possible, normal TUS) are shown in Figure 1. Fourteen patients in the "possible" category finally had PE, while 26 patients in this category had no PE.



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  		Figure 1.. Number of patients and results for different diagnostic criteria. US = ultrasound.

 

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  		Table 2.. TUS in the Diagnosis of PE

 

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  		Table 3.. Results of TUS for Diagnosing PE (n = 352)

 
The final diagnoses of patients not confirmed by CTPA may be considered weak. However, the TUS findings of patients with CTPA-confirmed PE did not differ notably extent from those diagnosed by a clinical algorithm (Table 4 ).


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  		Table 4.. Results of TUS by CTPA-Confirmed Diagnosis of PE (n = 325)

 
Localization: The majority (66%) of lesions were seen in the posterior basal segments of the lung (Fig 2 ).



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  		Figure 2.. Localization: The majority (66%) of lesions were seen in the posterior basal segments of the lung.

 
Number: In 144 of 194 patients, the sonograms demonstrated a total of 333 lesions (mean, 2.3 per patient) while CTPA showed 215 peripheral parenchymal lesions (mean, 1.5 per patient).

Size: The 328 ultrasound lesions on sonography averaged 15.5 x 12.4 mm in size (range, 5–62 x 5–70 mm), while the 215 consolidations on CTPA were 19.9 x 16.9 mm in size (range, 4–100 x 5–65). Sonography and CTPA were definitely concurrent with regard to the location of 101 lesions; the two procedures were also significantly concurrent with respect to the size of these lesions (p = 0.02, Spearman correlation coefficient). However, lesions are visualized larger on CTPA than on TUS (p = 0.0051, Wilcoxon signed-rank test).

Form: The sonographic morphology was mainly triangular toward the hilum of the lung in 58%, and rounded or mixed in 42% (Fig 3, 4 ). A small pleural effusion was seen in 49%, a basal effusion in 46 (33%), and a focal effusion in 23 (16%) of the cases.



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  		Figure 3.. Ultrasound image showing triangular lung (top) and rounded lung infarct (bottom). Both lesions are pleural based, open to transcutaneous ultrasound examination.

 


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  		Figure 4.. Thirty-six-year-old patient postoperatively. Top: PE confirmed in CTPA. Center: Triangular lesion on ultrasound. Bottom, left, c, and right, d: small rounded lesions on ultrasound.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Diagnostic procedures for PE still pose a challenge for the clinician. Thromboembolism is a dynamic event associated with recurrent embolization and spontaneous lysis. In terms of pathophysiology, 70 to 90% of thromboemboli are associated with peripheral pulmonary hemorrhages, so-called incomplete or partial infarctions, which may be reabsorbed within a few hours or days.2223 Therefore, it may be assumed that PE is still underestimated, underdiagnosed, and too rarely treated, even in a life-threatening situation.

One problem is that there is virtually no imaging "gold standard" available for clinical examination or daily practice. The dynamics of thromboembolism renders a comparison of methods difficult and limits any reference method. Therefore, in the present investigation, we used a time window of maximum 24 h for the reference method CTPA. Pulmonary angiography is rarely used because of its invasive nature and the risk of complications. Even with pulmonary angiography, the interobserver agreement for subsegmental emboli was only 66%.24 CTPA has been established as the first-line imaging procedure. However, only two thirds of patients who suffer from PE have a central demonstrable embolism.89

When the present study was designed at a conference in 2001, the following problem was encountered: while CTPA has been accepted as the principal method to diagnose PE and has replaced / scintigraphy in our institutions, the limitations of CTPA are well known.25 Small subsegmental lesions are considered to be irrelevant, although it is not known whether they are a harbinger of major PE. In the absence of a "gold standard," we had to use the best available procedure as the reference method. During the time period of the study, single-slice CTPA was available in all centers. The commonly used clinical algorithm was selected: CTPA was used as the primary reference method, while other methods (d-dimer, vein duplex sonography [VDUS], / scintigraphy, echocardiography, angiography of the pulmonary artery, biopsy) were used as often as possible and as frequently as needed in order to arrive at a conclusive clinical diagnosis.

In recent years, several efforts have been made to improve the diagnosis by the use of multislice CTPA. Multislice CTPA at thin collimation significantly improves the visualization of segmental and subsegmental arteries and reduces respiration and cardiac motion artifacts.1011 Peripheral lesions are often considered nonspecific, although their characteristic appearance has been known for > 15 years.26

In TUSPE, the diagnosis of PE was confirmed by SCTA in 169 patients (87%). The final diagnoses of patients not confirmed by SCTA may be considered weak. However, TUS findings for 25 patients (13%) with a diagnosis by a clinical algorithm using other methods were not notably different.

One fact that has received little attention is that transient hemorrhages and incomplete infarctions can be visualized by new imaging procedures (SCTA, TUS). On account of hemodynamics, peripheral hemorrhages and incomplete infarctions mainly occur in the lower lobes of the lung.2327 This phenomenon is helpful in ultrasound imaging, as is the fact that the lesions have a pleural base. In TUSPE, 66% of the demonstrated lesions were located in dorsobasal segments. This may be explained by the anatomy of the pulmonary arteries: they have a large axial trunk that branches off at an angle and terminates in the posterior basal segment. The emboli follow the axial flow.23 The lower lobes are easily viewed by TUS, while the upper lobes can only be inspected by an experienced investigator.

The fact that in acute PE, 2.3 lesions per patient are seen on sonography, vs 1.5 lesions on CTPA, is probably due to the time factor of spontaneous lysis until the CTPA is performed, and better resolution of ultrasonography in the subpleural region. Lesions visualized on TUS are smaller than on CTPA. At the deeper margins and the top of the infarct cone, air artifacts make the lesions appear smaller in sonography. However, TUS may depict a larger number of and smaller lesions than CTPA.

The large number (74%) of pulmonary hemorrhages and infarctions in our series of TUS is surprising but concurs with data reported in previous studies.18192021 In single-slice CTPA investigations,2829 wedge-shaped opacities have been described in 25 to 62% of small patient groups. When comparing different imaging modalities, the physical technical background should be taken into consideration. Due to reflection and absorption, ultrasound waves yield an entirely different picture of density compared to the images produced by electromagnetic waves in CT. Ultrasonography is superior to CT particularly in the close field, in terms of both spatial resolution and tissue differentiation. This is clearly evidenced in images of the cervical lymph nodes.

The sonomorphology of PE as opposed to inflammatory pulmonary conditions and neoplasms has been thoroughly investigated.172030 Although the specificity of individual lesions is limited, the following criteria may be recommended: two or more triangular or rounded lesions with a pleural base, 0.5 to 3 cm in size, may be regarded as confirmation of a clinically suspected PE. Two or more lesions were found in 44% of patients in TUSPE. However, Reissig and coworkers20 found two or more lesions in 74%. A typical pleural-based triangular or rounded lesion accompanied by a small pleural effusion makes a diagnosis of PE very likely. Subpleural lesions < 5 mm in size are very nonspecific and should not be considered as a PE.

The sonomorphology of consolidations due to other causes such as pneumonia or compression atelectasis must also be considered. A number of criteria may be used for sonomorphologic differential diagnosis between PE and peripheral pulmonary lesions of other origin. Pneumonias are larger, have blurred margins on the sonogram, are inhomogeneously structured, have numerous lenticular internal echoes, bronchoaerograms, and in cases of poststenotic pneumonias even fluid bronchograms. The echotexture of early pneumonia may be similar to that of liver tissue. Carcinomas and metastases are rather rounded or polycyclic, grow in an invasive fashion, have crow’s feet, tumor cones, and occasionally central necroses. Compression atelectases are narrow, shaped like a pointed cap, concave on at least one side, and float in the effusion.30 Peripheral venous malformation is very seldom and can be easily distinguished by color Doppler ultrasound.

Color-coded duplex sonography is a problematic procedure for diagnosing peripheral PE since many lesions tend to reperfuse early. However, in some cases, we find a characteristic circulation stop. The value of color-coded duplex sonography as one element in the mosaic of diagnostic procedures for PE needs to be investigated further. Ultrasound is more widely available than CTPA in European countries. With portable ultrasound systems, the patient can be examined at the bedside in ICU and emergency departments. In cases of pregnancy, contrast agent allergy, or renal failure, TUS may be an alternative to CTPA.

The TUSPE study shows that chest sonography may achieve importance in the diagnosis of PE because it can be applied at the bedside. However, a negative chest ultrasound result does not rule out a PE. Concurrent echocardiography and duplex sonography of the veins increase the diagnostic accuracy of sonographic procedures. The source, transmission, and arrival of thromboembolic disease can be detected with a single ultrasound system, thus "killing three birds with one stone."


   Acknowledgements
 
US: Bernd Braun MD Prof (Reutlingen), Otto Gehmacher MD (Hohenems), Uli Gehmacher MD (Hohenems), Alexander Kopf MD (Hohenems), Claus Kroegel MD Prof (Jena), Wilhelm Raneburger MD (Lienz), Bernhard Riedl MD (Lienz), Michael Scheier MD (Hohenems), Wolfgang Schröder MD (Reutlingen), Bernhard Schwärzler MD (Hohenems), Anton Theurl MD (Lienz), Alois Walder MD (Lienz), Andreas Werle MD (Hohenems), Oliver Wilhelm MD (Hohenems). CT and Scintigraphy: Wolfgang Doringer MD (Hohenems), Tanja Dütting MD (Reutlingen), Klaus Hergan MD (Hohenems), Jens-Peter Heyne MD (Jena), Peter Köstner MD, Adolf Lederer MD (Lienz), Martin Lenz MD (Reutlingen), Prof. Reinhard Loose MD Prof (Nürnberg), Manfred Oldendorf MD (Nürnberg). Data processing and preparation of the manuscript: Sujata Wagner (Wien), Judith Mathis (Rankweil), Michael Mathis (Rankweil), Robert Peschl MD (Hohenems). Statistical analysis: Hanno Ulmer Prof (Innsbruck).


   Footnotes
 
Abbreviations: CTPA = CT pulmonary angiography; PE = pulmonary embolism; TUS = thorax ultrasonography; TUSPE = thorax ultrasound in the diagnosis of pulmonary embolism; / = ventilation/perfusion

Received for publication September 22, 2004. Accepted for publication March 30, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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