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1
Department of Radiology, University René
Descartes-Paris V, Ambroise Paré Hospital, 9
Avenue Charles De Gaulle, 92104 Boulogne, France.
2
Medical Intensive Care Unit, University René
Descartes-Paris V, Ambroise Paré Hospital,
92104 Boulogne, France.
3
Department of Cardiology, University René
Descartes-Paris V, Ambroise Paré Hospital,
92104 Boulogne, France.
4
Department of Radiology, Centre Hospitalier de
L'Université de
Montréal, 1560 Sherbrooke E., Montreal, H2L
4M1, Canada.
Received February 28, 2000;
accepted after revision November 13, 2000.
Address correspondence to S. D. Qanadli.
Abstract
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MATERIALS AND METHODS. Fifty-four patients (mean age, 56 years) with
proven pulmonary emboli among 158 consecutive patients, who had undergone both
CT and pulmonary angiography for clinically suspected pulmonary embolism, were
eligible for the study. The CT obstruction index was defined as
(n · d) (n, value of the proximal
clot site, equal to the number of segmental branches arising distally;
d, degree of obstruction scored as partial obstruction [value of 1]
or total obstruction [value of 2]). We compared the CT obstruction index with
pulmonary arterial obstruction on angiography (assessed by the Miller index),
using linear regression, and correlated it with findings on echocardiography.
Interobserver variability was determined for both CT and pulmonary angiography
indexes.
RESULTS. The CT obstruction index (29% ± 17%) and the Miller index (43% ± 25%) were well correlated (r = 0.867, p < 0.0001) with an excellent concordance between investigators for both the CT index (r = 0.944, p < 0.0001) and the Miller index (r = 0.904, p < 0.0001). A CT obstruction index greater than 40% identified more than 90% of patients with right ventricular dilatation.
CONCLUSION. The degree of arterial obstruction in pulmonary embolism may be quantified by a specific CT index that appears reproducible and highly correlated to the previously described index with pulmonary angiography. Further evaluations are needed to investigate the usefulness of the CT obstruction index for stratification of patient risk and determining therapeutic options.
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The primary objective of our study was to define a specific index to quantify pulmonary arterial obstruction and to prospectively compare this index with a previously used angiographic index. The secondary objective was to determine whether the proposed index correlated with pulmonary arterial pressure and right ventricular function.
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All patients in our study received heparin therapy. The initial bolus dose was 5000 IU followed by a continuous infusion of 1000 IU/hr. The heparin dose was then adjusted to obtain a target of 1.5-2.5 times the normal activated clotting time. No patient received thrombolytic therapy.
The study was approved by our institutional ethics committee, and informed consent was obtained from all patients.
Helical CT and Obstruction Index Determination
CT scans were obtained with a CT Twin Flash scanner (Elscint, Haifa,
Israel), equipped with a double array of detectors, with the following
parameters: collimation, 5 mm (2 x 2.5 mm); table speed, 7.5 mm/sec
(pitch, 1.5); z-axis coverage, 15 cm. Images were acquired in the
caudocranial direction to allow imaging of the main, lobar, segmental, and
subsegmental arteries of the lower, middle, and upper lobes. Images were
reconstructed at 1.3-mm intervals with 180° linear interpolation with
effective slice thickness of 2.7 mm and were archived on an optical cartridge.
A total of 120-150 mL of 250 mg I/mL iobitridol (Xenetix 250; Guerbet,
Aulnay-sous-Bois, France) was injected at a rate of 4 mL/sec and a scan delay
of 10-15 sec.
The helical CT criterion used to diagnose pulmonary emboli consisted of direct visualization of nonocclusive endoluminal thrombus (central filling defect completely or partially outlined by contrast agent) or of complete occlusion by thrombus in normal-sized or enlarged vessels.
CT scans were reviewed on an independent workstation (OmniView or OmniPro; Elscint) independently by two investigators experienced in reviewing helical CT and blinded to the selective pulmonary angiography findings. Each investigator was asked to score vascular obstruction. To define the CT obstruction index, the arterial tree of each lung was regarded as having 10 segmental arteries (three to the upper lobes, two to the middle lobe and to the lingula, and five to the lower lobes). The presence of embolus in a segmental artery was scored 1 point (Fig. 1A,1B), and emboli in the most proximal arterial level were scored a value equal to the number of segmental arteries arising distally (Figs. 2A,2B,2C and 3A,3B,3C,3D). To provide additional information about the residual perfusion distal to the embolus, a weighting factor was assigned to each value, depending on the degree of vascular obstruction. This factor was equal to zero, when no thrombus was observed; 1, when partially occlusive thrombus was observed (Figs. 1A,1B and 2A,2B,2C); or 2, with total occlusion (Figs. 1A,1B and 3A,3B,3C,3D). Thus, the maximal CT obstruction index was 40 per patient. Isolated subsegmental embolus was considered as a partially occluded segmental artery and was assigned a value of 1.
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The percentage of vascular obstruction was calculated by dividing the
patient score by the maximal total score and by multiplying the result by 100.
Therefore, the CT obstruction index can be expressed as: (n
· d) / 40 x 100, where n is the value of the
proximal thrombus in the pulmonary arterial tree equal to the number of
segmental branches arising distally (minimum, 1; maximum, 20), and d
is the degree of obstruction (minimum, 0; maximum, 2).
Selective Pulmonary Angiography Protocols and the Miller Score
Determination
Pulmonary angiography with a digital subtraction system (Integris; Philips
Medical Systems, Best, The Netherlands) was performed in all patients with a
standard Seldinger femoral approach and local anesthesia. The right and the
left pulmonary arteries were selectively catheterized with a 6-French multiple
side-hole Grollman catheter (Cook, Eindhoven, The Netherlands). Angiograms
were obtained at a rate of five frames per second after injection of 35-40 mL
of 300 mg I/mL iobitridol (Xenetix 300; Guerbet) or 320 mg I/mL ioxaglate
(Hexabrix 320; Guerbet) at a flow rate of 15-20 mL/sec. A minimum of two
selective angiograms (anteroposterior and oblique projections) was obtained
per lung. Measurement of the mean pulmonary arterial pressure was obtained in
35 patients before angiography. All Patients received oxygen with a mask (4-10
L/min) during and after selective pulmonary angiography.
Embolism was diagnosed on selective pulmonary angiography if an intraluminal filling defect or a cutoff in a vessel measuring at least 2 mm in diameter was seen [11].
Pulmonary angiograms were independently reviewed on hard copy and on the computer screen of a digital compact disc archiving workstation (Sparc Station 5; Medical Electronics Vertriebs-GmbH, Weisbaden, Germany) by two other investigators who were unaware of the CT findings. Each investigator independently scored the pulmonary arterial obstruction, using the angiographic index described by Miller et al. [12]. The Miller index is composed of a score for arterial obstruction (objective score) and a score for reduction of the peripheral perfusion of the lungs (subjective evaluation). The right pulmonary artery is assigned nine segmental arteries (three to the upper lobe, two to the middle lobe, and four to the lower lobe), whereas the left pulmonary artery is assigned only seven segmental arteries (two to the upper lobe, two to the lingula, and three to the lower lobe). The presence of segmental emboli, regardless of the degree of obstruction, is scored 1 point (Fig. 1A,1B). Proximal emboli to the segmental level are scored a value equal to the number of segmental arteries arising distally according to the predetermined anatomic subdivisions described previously (Figs. 2A,2B,2C and 3A,3B,3C,3D). The maximal score of obstruction is 16. Reduction of peripheral perfusion is scored by dividing each lung into upper, middle, and lower zones and by using a four-point scale: 0 points, in case of normal perfusion; 1 point, when the perfusion is moderately reduced; 2 points, when the perfusion is severely reduced; 3 points when the perfusion is absent. The maximal score of reduced perfusion is 18. Thus, the maximal Miller index is 34 per patient.
The percentage of vascular obstruction was calculated in the same manner as that for the CT obstruction index by dividing the patient score by the maximal total score (34) and by multiplying the result by 100.
Echocardiography
Two-dimensional transthoracic echocardiography was performed with Apogec CX
200 (Advanced Technology Laboratories, Bothell, WA) and Power Vision 6000
(Toshiba; Puteaux, France) ultrasound systems interfaced with 3.5- and 3-MHz
transducers, respectively. All examinations were videotaped and analyzed by
experienced echocardiographers who were unaware of the CT obstruction index
and the Miller index scores. Quantitative assessment of the right ventricle
was obtained by measuring the end-diastolic right ventricular area on the
apical four-chamber image. A ratio of end-diastolic right ventricle area to
end-diastolic left ventricle area greater or equal to 0:6 indicated right
ventricle dilatation [13].
Statistical Analysis
Results are expressed as mean ± standard deviation. The percentage
of vascular obstruction reported was the mean of the evaluations of the two
independent investigators. Significance of the relationship between
angiographic findings (the Miller index and mean pulmonary arterial pressure)
and CT findings (the CT obstruction index) was assessed by regression
analysis. Interobserver variability was determined for both CT and
angiographic indexes and subsequently analyzed by linear regression equations.
Confidence intervals of 95% for coefficients of correlation were estimated. A
p value less than 0.05 was considered statistically significant.
Statistical analysis was performed with a statistical software system
(StatView for Macintosh, version 4.5; Abacus Concepts, Berkeley, CA).
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The obstruction CT index determination disclosed a mean value of 29% ± 17% (range, 2.5-57.5%). The mean percentage of vascular obstruction expressed by the CT obstruction index was inferior to that expressed by the Miller index. There was an excellent correlation between both investigators (r = 0.944, p < 0.0001). The mean difference between CT investigators was 4% (maximum of 20%), whereas it was 9% (maximum of 30%) between selective pulmonary angiography investigators.
A statistically significant relationship was found between the mean percentage of vascular obstruction by CT and by selective pulmonary angiography (r = 0.867, p < 0.0001). Table 1 provides correlation coefficients among investigators.
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Pulmonary arterial hypertension (mean pulmonary arterial pressure, >20 mm Hg) was observed in 25 patients. A poor correlation (r = 0.534, p = 0.0008) was found between mean pulmonary arterial pressure and the Miller index in the subgroup of patients who had pulmonary pressure measurements. Similarly, low correlation was found between the CT obstruction index and mean pulmonary arterial pressure (r = 0.584, p = 0.0002).
Among the 20 patients who underwent echocardiography, 10 patients had evidence of right ventricle dilatation (ratio of right ventricle to left ventricle, >0.6). Figure 4 shows the relationship between the percentage of obstruction obtained by both the Miller index and the CT obstruction index and right ventricle dilatation. Nine patients (91%) with a ratio of right ventricle to left ventricle greater than 0.6 had pulmonary vascular obstruction greater than or equal to 40%, and all patients with a ratio of right ventricle to left ventricle of less than 0.6 had less than 40% pulmonary vascular obstruction expressed by both the CT obstruction index and the Miller index. Only one patient had a ratio of right ventricle to left ventricle greater than 0.6 with a mean pulmonary arterial pressure of 29 mm Hg and a CT obstruction index of 18%. All patients with a ratio of right ventricle to left ventricle of 0.6 or greater had a mean pulmonary arterial pressure greater than 20 mm Hg. In contrast, three patients with mean pulmonary arterial pressure greater than 20 mm Hg had a ratio of right ventricle to left ventricle of less than 0.6.
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Bankier et al. [16] have applied two angiographic indexes, the Miller index and the Walsh scores [17], to helical CT to quantify the severity of pulmonary obstruction. However, the original scoring system of Miller et al. [12] was modified to be applied to helical CT. Subsequently, only the obstruction component of the Miller index was used. Thus, no indication about residual perfusion of the lung was taken into account. In this system, the presence of nonobstructive clots in the main pulmonary arteries corresponds to a percentage of obstruction of 100%, which is not necessarily consistent with clinical severity (Fig. 2A,2B,2C). Moreover, the Walsh scoring system is more complex to calculate and, consequently, has rarely been used in clinical practice. For these reasons, we designed a new index dedicated to a noninvasive sectional imaging technique, such as helical CT, to quantify pulmonary vascular obstruction, integrating residual perfusion in the pulmonary arterial tree. Differentiation between complete and partial obstruction by the proximal clot may add relevant information about the residual perfusion of the lung (Fig. 3A,3B,3C,3D).
Our data show that the defined index is simple and reproducible. By design, this index is based on the number of segmental arteries that contained thrombus or that arose distal to a thrombus located in a more proximal branch. Subsequently, this index is easy to calculate even in cases with anatomic variations. A high degree of agreement between investigators in determining the CT obstruction index and a high degree of correlation between the CT obstruction index and the Miller index was found. The mean percentage of vascular obstruction expressed by the CT obstruction index was inferior to that expressed by the Miller index. This variation could be explained by differences in design of the two indexes. Compared with the Miller index, the weighting system used in our CT index underestimated the score (expressed in percentage of obstruction), especially in proximal emboli, which rarely caused total obstruction (Fig. 2A,2B,2C). The subjective component of the Miller index provided a high value of perfusion defect, resulting in a higher score than that on CT. In fact, a proximal partially occlusive embolus, with a weighting factor of 1 of CT, could be associated with more distal occlusive emboli that alter parenchymal perfusion on selective pulmonary angiography (Fig. 2A,2B,2C). However, subjective evaluation of the residual perfusion of the lung on selective pulmonary angiography may lead to interobserver variability. This observation could explain why a lower correlation was observed between selective pulmonary angiography investigators than between CT investigators (Figs. 2A,2B,2C and 3A,3B,3C,3D).
The CT obstruction index and the Miller index were poorly correlated to the mean pulmonary arterial pressure in our study group. Obstruction of the pulmonary vascular tree is the main factor in increased pulmonary vascular resistance, resulting in pulmonary hypertension in patients with acute pulmonary embolism [18, 19]. The role of reflex vasoconstriction, which accompanies mechanical obstruction, in the pathogenesis of pulmonary hypertension remains unclear. However, the hemodynamic profile may depend on the presence or absence of preexisting pulmonary disease [20]. Better correlation between mean pulmonary arterial pressure and the severity of obstruction was reported in selected patients without underlying pulmonary disease [21], compared with unselected patients [22], as was the case in our study group. However, this preliminary report is limited by the fact that only 35 patients had measurements of the pulmonary artery pressure, and more experience is needed to confirm these data.
It is important to show the relationship between the CT obstruction index and other parameters (e.g., those recently used in stratification of patient risk, such as right ventricular dilatation). The presence of right ventricular dysfunction may indicate a high likelihood of recurrent and possibly fatal pulmonary embolism, despite adequate anticoagulation therapy [14, 23]. The degree of pulmonary vascular obstruction is considered the most important factor determining the right ventricular response to acute pulmonary embolism [24]. Our data suggest that the CT obstruction index could predict right ventricular dilatation. A CT obstruction of 40% or greater will identify more than 90% of patients with right ventricular dilatation. Alternately, a CT obstruction index of less than 40% would be unlikely in the presence of a pulmonary embolism with acute right ventricular dysfunction. These results are consistent with previously reported data on selective pulmonary angiography [25].
A criticism of our preliminary experience is that patients with clinical signs of severe pulmonary embolism requiring thrombolytic therapy could not be enrolled because both CT and selective pulmonary angiography could not be performed in patients with this condition. Furthermore, as previously indicated, all included patients could not undergo echocardiography and pulmonary artery pressure measurements. Thus, more experience is needed to confirm the reported data and to determine whether this index could predict right ventricle dysfunction. The clinical significance of the CT obstruction index in regard to prognostic value and therapeutic options should also be assessed.
In conclusion, helical CT has been recently introduced in diagnostic strategies of pulmonary embolism as a noninvasive test with a high accuracy. This observation requires that we expand our concept of "detection of pulmonary embolism" to include evaluation of the degree of vascular obstruction. The specific index (the CT obstruction index) that we propose to quantify vascular obstruction in helical CT appears simple, reproducible, and highly correlated to a previously described index with selective pulmonary angiography. The CT obstruction index could be used to grade the severity of pulmonary embolism and to monitor patients requiring an objective repetitive evaluation. However, further evaluations are needed to investigate the usefulness of the CT obstruction index for determining stratification of patient risk and influencing therapeutic decisions.
Acknowledgments
We thank Jean-Pierre Bourdarias, Jean-Christophe Boulard, Dominique
Brun-Ney, Thierry Chinet, and François Jardin
for their support and advice.
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