Pulmonary Embolism Outcome: A Prospective Evaluation of CT Pulmonary Angiographic Clot Burden Score and ECG Score

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1 Chest Imaging Original Research Subramaniam et al. Pulmonary Embolism Outcome Chest Imaging Original Research Downloaded from by on 1/28/18 from IP address Copyright ARRS. For personal use only; all rights reserved Rathan M. Subramaniam 1,2 Jay Mandrekar 3 Catherine Chang 4 Damon Blair 1 Kevin Gilbert 1 Patrick J. Peller 2 Jamie Sleigh Noel Karalus 4 Subramaniam RM, Mandrekar J, Chang C, et al. Keywords: CT angiography, CT pulmonary angiographic clot burden score, ECG score, outcome, pulmonary embolism, thorax DOI:1.2214/AJR Received July 11, 27; accepted after revision December 17, 27. Supported by two research grants (22 and 24) from the Waikato Medical Research Foundation, Hamilton, New Zealand. This work was carried out at the Department of Respiratory Medicine and the Department of Radiology, Waikato Hospital, Hamilton, New Zealand. The statistical analysis for the manuscript was performed in the Department of Biostatistics and Health Services Research, Mayo Clinic, Rochester, MN. 1 Department of Radiology, Waikato Hospital and Waikato Clinical School, University of Auckland, Hamilton, New Zealand. 2 Department of Radiology, Mayo Clinic and Mayo College of Medicine, 2 1st St. SW, Rochester, MN 9. Address correspondence to P. J. Peller (peller.patrick@mayo.edu). 3 Department of Biostatistics and Health Services Research, Mayo Clinic and Mayo College of Medicine, Rochester, MN. 4 Department of Respiratory Medicine, Waikato Hospital, Hamilton, New Zealand. Department of Intensive Care, Waikato Hospital and Waikato Clinical School, University of Auckland, Hamilton, New Zealand. CME This article is available for CME credit. See for more information. AJR 28; 19: X/8/ American Roentgen Ray Society Pulmonary Embolism Outcome: A Prospective Evaluation of CT Pulmonary Angiographic Clot Burden Score and ECG Score OBJECTIVE. The purpose of this study was to establish whether a correlation exists between the CT pulmonary angiographic clot burden score, the ECG score at diagnosis, and the 12-month mortality rate among patients diagnosed with pulmonary embolism. SUBJECTS AND Methods. A total of 23 consecutive patients who underwent CT pulmonary angiography for a suspected moderate to high pretest probability of pulmonary embolism were recruited from March 23 to October 24. There were 1 patients with positive CT pulmonary angiography examinations. Two consultant respiratory physicians and two consultant radiologists independently and prospectively calculated an ECG score and a quantified pulmonary artery clot burden, respectively. Twelve-month follow-up was completed in all patients. RESULTS. The mean ECG score was 2.36 (SD, 2.84) and the mean clot burden score percentage was 23.74% (16.8%). Poor correlation (r =.9) was seen between the average ECG score and the average clot burden score percentage (p =.39) at diagnosis. Thirteen patients had died at the 12-month follow-up. The mean ECG score for those patients who were alive was 2.4 (2.91) and for those who had died was 2.3 (2.34) at 12 months (p =.6). The mean clot burden score percentage for those patients who were alive was 24% (17%) and for those who had died was 22.1% (1.7%) at 12 months (p <.73). CONCLUSION. No statistically significant association was seen between ECG score and CT pulmonary angiographic clot burden at diagnosis and the 12-month all-cause mortality rate of patients diagnosed with pulmonary embolism. P ulmonary embolism is a common and potentially fatal disease with a mortality of 2 7%, even when treated with anticoagulation [1 3]. The introduction of helical CT has considerably modified the diagnostic approach to acute pulmonary embolism, and its accuracy has increased parallel with the improvements in CT technology over the years [4 6]. In routine clinical practice, CT pulmonary angio graphy is mainly used as a diagnostic test. It allows not only a noninvasive depiction of endoluminal thrombus but also the identification of other, nonembolic causes of thoracic symptoms [7 9]. Consequently, CT pulmonary angiography has become the first-line imaging examination performed in patients suspected of having acute pulmonary embolism [1, 11]. Anticoagulation can be withheld safely in patients who have a negative CT pulmonary angiographic examination [12, 13]. Multiple retrospective studies have evaluated the accuracy of CT pulmonary angiographic clot burden scores [14 22]. Only a few of these retrospective studies have investigated the relationship between the clot burden score and patient outcome [19 22]. The literature contains discrepancies regarding the potential for association between the severity of pulmonary angiographic clot burden and the immediate outcome [23]. Studies to date are limited by their retrospective nature and the small number of patients investigated. The association between the intermediate and long-term outcomes and the severity of pulmonary angiographic clot burden at diagnosis is not known. Daniel et al. [24] established an ECG score that increases with pulmonary hypertension due to pulmonary embolism. A score of greater than 1 is suggestive of severe pulmonary hypertension. This ECG score also predicted those with the greatest percentage of perfusion defects on ventilation perfusion examinations [2]. But whether this ECG score has any correlation with the embolic clot burden at diagnosis or association with outcome (as measured by mortality rate) is not known. AJR:19, June

2 Subramaniam et al. Downloaded from by on 1/28/18 from IP address Copyright ARRS. For personal use only; all rights reserved The objectives of this study were to prospectively evaluate whether a correlation exists between the ECG score [24] and the CT pulmonary angiography clot burden score [1] at diagnosis and to evaluate any potential association between the scores and the 12-month all-cause mortality rate among patients diagnosed with pulmonary embolism. Subjects and Methods Patients Regional ethics committee approval was obtained and all enrolled patients completed a written consent form. Five hundred twenty-three consecutive patients (both inpatients and em ergency department outpatients) with a sus pected moderate to high pretest probability for pulmonary embolism (clinical suspicion and at least one of the major risk factors for pulmonary embolism per British Thoracic Society guidelines [26] or positive D-dimer assay) were prospec tively re cruited to the study from March 23 to October 24, in a tertiary center. Patients with a low pretest clinical pro bability for pulmonary em bolism (no major risk factor for pulmonary embolism of the British Thoracic Society guideline and a negative D-dimer assay) were excluded from the study as unlikely to have pulmonary embolism, according to local clinical practice. The 23 patients had a median age of 8 years (range, years). There were 284 (4.3%) females and 239 (4.7%) males. Two hundred sixtyseven (1%) patients were referred from the emergency department; 121(23%) from medical specialists, and 13 (26%) from surgical specialists. The study population included 18 patients with active cancer. Patients were examined by physicians, and baseline investigations (chest radio graph, ECG, and arterial blood gases) were per formed in all patients before CT pulmonary angiography. CT Pulmonary Angiography CT pulmonary angiography was performed using a single-detector helical scanner (HiSpeed CT/i, GE Healthcare). A contrast-enhanced CT evaluation of the pulmonary arteries was performed in a caudocranial direction from the top of the diaphragm to the level of the aortic arch. Scans were acquired during a single breath-hold or shallow breathing, depending on the patient s ability to hold his or her breath during the acquisition time. Scans were obtained at 3-mm collimation and pitch and were reconstructed at 1.-mm intervals using a standard algorithm. Contrast material was injected via an 18- to 2-gauge cannula in an antecubital vein and both arms were placed above the patient s head. A total volume of 1 ml of nonionic contrast material ([iohexol], Omnipaque 3, GE Healthcare, formerly Nycomed) was injected at a rate of 4. ml/s. Scanning began when the contrast material was first seen in the pulmonary trunk using a bolus-tracking software (SmartPrep, GE Healthcare). CT Pulmonary Angiographic Readings Images were reviewed on a workstation at settings for pulmonary vasculature (window width, 4 H; window level, H) and lung parenchyma (window width, 1,2 H; window level, 7 H). The presence or absence of occlusive or nonocclusive thrombus in the main, lobar, segmental, and subsegmental arteries was recorded. The studies were classified as positive for pulmonary embolism if thrombus was observed; negative for pulmonary embolism if no thrombus was observed; or indeterminate if a poor examination, poor contrast enhancement, or motion artifacts precluded confident interpretation of the study. Helical CT Criteria for Scoring Vascular Obstruction All CT pulmonary angiographic examinations were independently read by two radiologists, and clot burden scores [1] were calculated prospectively for all 1 patients with positive CT pulmonary angiographic examinations for pulmonary embolism. Qanadli et al. [1] evaluated a specific index for quantifying arterial obstruction with helical CT in acute pulmonary embolism and showed that their proposed score was reproducible and correlated highly to the pul monary angiography index. In this study, we used the same scoring system based on the site of obstruction and the degree of occlusion of the pulmonary arteries. Site of obstruction The presence of thrombus in a segmental artery received a point value of 1. Emboli in the most proximal arterial level received a total score equal to the number of segmental arteries arising distally, according to the predetermined anatomic subdivisions described previously (maxi mum score of 3 for the upper lobe arteries, 2 for the middle lobe and the lingual arteries, for the lower lobe arteries, 7 for the intermediate arteries, and 1 for the main pulmonary arteries). A single filling defect extending into more than one anatomic location was scored for each location up to, but not exceeding, the maximum designated for each region. The maxi mum possible score for involvement was 2 points [1]. Degree of obstruction In addition to assessing the level of obstruction, and to provide additional information about the perfusion distal to the thrombus, we multiplied all scores related to the level of obstruction by a weighting factor ( 1 when the thrombus was partially occlusive; 2 when the thrombus was totally occlusive), depending on the degree of vascular obstruction caused by embolism [1]. Each obstruction therefore received a score depending on the vessel involved multiplied by the weighting factor. The value of the most proximal thrombus in the pulmonary arterial tree scored a maximum of 6 (3 2) for the upper lobe arteries, 4 (2 2) for the middle lobe and the lingual arteries, 1 ( 2) for the lower lobe arteries, 14 (7 2) for the intermediate arteries, and 2 (1 2) for the main pulmonary arteries; thus, the maximal CT obstruction score for any patient could not exceed 4. Percentages were calculated from the raw scores. ECG ECG was performed in all patients as part of the clinical assessment before CT pulmonary angiography was performed. Two respiratory physicians scored each ECG examination independently according to a previously established scoring system [2] (Table 1) in those patients who were diagnosed with pulmonary embolism on CT pulmonary angiography. The ECG readers were blinded to the clot burden scores calculated by the two radiologists but were aware that patients were diagnosed with pulmonary embolism on CT pulmonary angiography. TABLE 1: ECG Scoring System ECG Characteristic Score Tachycardia (> 1 beats per minute) 2 Incomplete right bundle branch block 2 Complete right bundle branch block 3 T wave inversion in leads V 1 V 4 4 T wave inversion in lead V 1 (mm) < > 2 2 T wave inversion in lead V 2 (mm) < > 2 3 T wave inversion in lead V 3 (mm) < > 2 3 S wave in lead V 1 Q wave in lead V 3 1 Inverted T wave in lead V 3 1 If all of S 1 Q 3 T 3 2 Note Maximum total score is 21. S 1 Q 3 T 3 = S wave in lead V 1, Q wave in lead V 3, and T wave inversion in lead V 3. Adapted from [2]. 16 AJR:19, June 28

3 Pulmonary Embolism Outcome Downloaded from by on 1/28/18 from IP address Copyright ARRS. For personal use only; all rights reserved Follow-Up and Outcome Patients were interviewed by two research nurses and a radiologist at the end of 3 and 12 months, by telephone, to establish whether the patients were alive or had died during the follow-up. In instances in which patients could not be contacted, the family medicine practitioner was contacted. Clinical records and death certificates were reviewed by a radiologist if the patient had died during the follow-up period. The patient outcome was defined as all-cause mortality at 12-month follow-up. This definition indicates death of study patients within 12 months from the date of CT pulmonary angiography diagnosis of pulmonary embolism due to any medical cause rather than specifically pulmonary embolism. Statistical Analysis Categoric variables of patient demographics, presentations, and comorbid conditions are summarized as frequencies and percentages. Continuous variables such as age, ECG scores, and clot burden score percentages are summarized as median and minimum, maximum. Box plots were used to present the distribution of ECG scores and clot burden score percentages between the patient cohort who had died and the patient cohort who were alive at the 12-month follow-up. Comparison of the ECG scores and clot burden score percentages between those who were alive and those who were dead at 12 months was done using Wilcoxon s rank sum test because of the nongaussian distribution of the data. Linear associations between the ECG scores calculated by two respiratory physicians, clot burden score percentages calculated by two radiologists, and the association between the ECG scores and the clot burden score percentages were assessed graphically using scatterplots, and the degree of this association was estimated using Pearson s correlation coefficient as appropriate. All the statistical tests were twosided, and a p value less than. was considered statistically significant. The agreement between ECG scores calculated by the two physicians and the clot burden score percentages calculated by the two radiologists were assessed using intraclass correlation [27], and appropriate 9% CIs were estimated. All statistical analyses were performed using a commercially available software program (SAS, version 8.; SAS Institute). Results Patients Among the 1 patients diagnosed with pulmonary embolism who completed the 3- and 12-month follow-up were 46 females and 9 males having a median age of 8 years (age range, years). Twenty-two patients had a history of previous deep vein thrombosis or pulmonary embolism, and 18 patients had a history TABLE 2: Cause and Time of Death in Patients Who Died During 12-Month Follow-Up Patient No. Cause of Death Time a 1 Possible pulmonary embolism < 7 d 2 Pneumonia < 1 mo 3 Severe COPD < 1 mo 4 Malignancy 1 3 mo Malignancy 1 3 mo 6 Heart failure 1 3 mo 7 Malignancy 1 3 mo 8 Malignancy 3 12 mo 9 Cerebrovascular incident 3 12 mo 1 Heart failure 3 12 mo 11 Pneumonia 3 12 mo 12 Malignancy 3 12 mo 13 Heart failure 3 12 mo Note COPD = chronic obstructive pulmonary disease. a Since beginning of study. of active malignancy [13]. Thirteen patients died during the 12-month follow-up period; the cause and time of death are outlined in Table 2. Patient Outcome and the Average Clot Burden Score Percentages The mean CT pulmonary angiographic clot burden score percentage was 23.74% (SD, 16.8%; range, %). Excellent intraclass correlation of.91 (9% CI,.89.92) was seen, as was a good Pearson s correlation of.72 (p <.1) between the Radiologist 1 Score (%) Radiologist 2 Score (%) two radiologists calculations of clot burden score percentages (Fig. 1). The mean clot burden score percentage for patients who were alive was 24% (SD, 17%; range, %) and for those who had died was 22.1% (1.7%; range, %) at the 12-month (p <.73) follow-up (Fig. 2). Patient Outcome and ECG Scores The mean ECG score was 2.36 (2.84; range,. 16.) for the patients diagnosed with pulmonary embolism. Excellent intraclass correlation of.96 (9% CI,.9.96) was seen, as was excellent Pearson s correlation of r =.89 (p <.1) between the two physicians calculations of ECG scores (Fig. 3). The mean ECG score for patients who were alive at 12 months was 2.4 (2.91; range, ) and for those who died was 2.3 (2.34; range, 2. 7.) (p =.6) (Fig. 4). Correlation Between ECG Score and Clot Burden Score We divided the patients into three groups based on the quantity of clot burden: < 3%, 3 %, and > %. The respective mean ECG scores were 2.8 (median, 1.; SD, 2.9), 3. (median, 2.; SD, 3.3), 1.9 (median,.; SD, 2.48) (Fig. ). Poor correlation (r =.9) occurred between the average ECG score and the average clot burden score percentage (p =.39) (Fig. 6). Univariate analysis (Table 3) identified active malignancy (odds ratio [OR],.8; p <.1) and surgery within 6 weeks (OR, 9.64; p =.3) as the only patient characteristics significantly associated with mortality at 12 months among the pulmonary embolism positive cohort patients. Diastolic blood pres- 8 1 Fig. 1 Clot burden score percentages calculated by reader 1 are plotted on y-axis and those calculated by reader 2 on x-axis. Intraclass correlation was.91 (9% CI,.89.92); Spearman s correlation was.72 (p <.1). AJR:19, June

4 Subramaniam et al. Downloaded from by on 1/28/18 from IP address Copyright ARRS. For personal use only; all rights reserved Average Clot Burden Score (%) Alive Dead 12-Month Follow-Up Fig. 2 Outcome at 12-month follow-up and average clot burden score percentage (p <.73). sure < 7 mm Hg at presentation (OR, 3.9; p =.6) may also have an association with the mortality rate at 12 months. Discussion One reason to risk-stratify patients who are suspected early in their presentation of having pulmonary embolism is to identify those patients with acute massive or submassive pulmonary embolism who may benefit from thrombolysis [28]. Conversely, those with non-life-threatening pulmonary embolism can be treated with anticoagulation as outpatients [29]. Previously identified methods that define the severity of pulmonary embolism, such as the findings of right ventricular dysfunction on echocardiography, are not routinely available in most centers for the early management of the patients with possible pulmonary embolism. Hence, there is a need to develop strategies that quickly and noninvasively identify patients with a significant thrombus burden and to apply those strategies routinely in the early assessment of pulmonary embolism. The pulmonary arterial obstruction index used in this study is based on the description by Qanadli et al. [1], in which the segmental pulmonary arteries are the basic units for scoring, and a weighted factor is considered for occlusive versus nonocclusive emboli. We report a mean percentage of pulmonary arterial obstruction of 23.7% (range, %), which is similar to the figure (22%) described by Wu et al. [19] and lower than Reader 1 ECG Score Reader 2 ECG Score Average ECG Score (%) Dead Alive 12-Month Follow-Up Fig. 4 Outcome at 12-month follow-up and average ECG score (p <.23). 1 2 Fig. 3 ECG scores calculated by reader 1 are plotted on y-axis and those calculated by reader 2 on x-axis. Intraclass correlation was.96 (9% CI,.9.96); Pearson s correlation was r =.89 (p <.1). the figure described by Qanadli et al. (29%). This difference may be due to differences in the demographics of the patients studied. Our study showed no statistically significant correlation between the pulmonary angiographic clot burden score calculated according to Qanadli et al. [1] and the 12-month all-cause mortality rate. This result may be due to a selection bias, in that patients with a large clot burden may have died before CT pulmonary angiography was performed, so that patients with pulmonary embolism who survive to undergo CT pulmonary angiography have less severe clot burden. Although other studies have reported pulmonary angiographic clot burden scores to be a poor predictor of short-term mortality in patients with acute pulmonary embolism [18, 21], to our knowledge, no studies in the literature examine the potential association between the CT pulmonary angiographic clot burden at diagnosis and the intermediate outcome (such as 12-month mortality rate). Two small retrospective studies have suggested a correlation between the CT pulmonary angiographic clot burden and patient shortterm mortality [19, 2]. Wu et al. [19] reported that patients with a pulmonary angiographic clot score of more than 6% tended to die. Those authors [19] and van der Meer et al. [2] Average ECG Score (%) <3% 3 % > % Clot Burden Categories Fig. Average ECG scores and three categories of CT pulmonary angiographic clot burden score (< 3%, 3 %, and > %). 162 AJR:19, June 28

5 Pulmonary Embolism Outcome Downloaded from by on 1/28/18 from IP address Copyright ARRS. For personal use only; all rights reserved Averaage ECG Score Average Clot Burden Score (%) found the clot burden score proposed by Qanadli et al. [1] to be a significant predictor of death, with positive results at CT pulmonary angiography (p <.2). The median clot burden score for our cohort is 21%, which is similar to that obtained by Wu et al. and van der Meer et al. (1% and 32%, respectively). This supports that selection bias is unlikely to be an important confounder in our cohort. In addition, our study showed all patients who had died at 3 or 12 months had a CT pulmonary angiographic clot burden of less than 4%. Two dedicated CT pulmonary angiographic scoring systems are available, as proposed by 8 Fig. 6 Scatterplot shows poor correlation between average ECG score and average clot burden score percentage (r =.9; p =.39). TABLE 3: Univariate Analysis of Comorbid Conditions and 12-Month Mortality Rate Patient No. Condition Odds Ratio Lower 9% CI Upper 1 Recent surgery a Diastolic blood pressure < 7 mm Hg Systolic blood pressure > 14 mm Hg PaO 2 < 6 mm Hg Previous PE or DVT COPD Clot burden History of smoking Heart failure History of myocardial infarction Male sex Age > 6 years Active malignancy a <.1 Note PE = pulmonary embolism, DVT = deep venous thrombosis, COPD = chronic obstructive pulmonary disease. a Significantly associated with 12-month all-cause mortality rate in patients diagnosed as having pulmonary embolism. p Qanadli et al. [1] and Mastora et al. [16]. We used the system developed by Qanadli et al. because it was the scoring system available at the time our study was planned in 22. A recent retrospective study involving 89 patients diagnosed with pulmonary embolism concluded that the Mastora obstruction score showed a significant correlation with early death within 3 days, whereas the Qanadli pulmonary embolism obstruction score showed no significant correlation with 3-day mortality [22]. Although both scores are simple to use and reproducible, the Mastora obstruction score is significantly varied (analysis of variance, p <.1) and lower than the Qanadli obstruction score used in this study. This is most likely due to differences in calculation of clot burden in these scoring models. A number of ECG changes have been associated with severity of pulmonary embolism and outcome [3 32]. The ECG scoring system developed by Daniel et al. [24] increases with severity of pulmonary hypertension due to pulmonary embolism and also predicts those with the greatest percentage of perfusion defect on ventilation perfusion examinations [2]. Iles et al. [2] retrospectively recruited 229 patients who had pulmonary embolism diagnosed on ventilation perfusion scans and ECG performed within 48 hours of the lung scans. The mean ECG scores were 2.6, 3.2, and.3 in patients with < 3%, 3 %, and > % perfusion defects on the ventilation perfusion scans, respectively. In comparison, our patients were prospectively recruited, ECG was performed before CT pulmonary angiography on the same day, and the diagnosis of pulmonary embolism was made on CT pulmonary angiograms. Our study showed a poor correlation between the ECG scores and the CT pulmonary angiographic clot burden at diagnosis. Our study also suggests that no statistically significant association exists between the ECG score and the 12-month mortality rate. To our knowledge, ours is the first prospective study examining the correlation between ECG score and CT pulmonary angiographic clot burden at diagnosis and the 12-month mortality rate. This prospective study refutes the hypothesis that ECG changes and pulmonary artery clot burden at diagnosis may be useful in risk-stratifying and prognosis of patients diagnosed with pulmonary embolism. This is in contrast to previous promising findings of using ECG scoring and pulmonary angiographic clot burden as tools for risk stratification or prognosis in patients with pulmonary embolism. Our results are likely due to patient outcome or because death is determined by a combination of other comorbidities such as malignancy or surgery, rather than the diagnosis of pulmonary embolism itself. Our study had some limitations. First, we analyzed the ECG studies only of patients who were diagnosed with pulmonary embolism on CT pulmonary angiography. Second, the ECG scoring system we used may have its own limitation because it is largely based on T wave inversion, which may vary as a result of right bundle branch block; these inversions are frequently found in leads V 1 and AJR:19, June

6 Subramaniam et al. Downloaded from by on 1/28/18 from IP address Copyright ARRS. For personal use only; all rights reserved V 3 of healthy individuals. Third, we used single-detector helical CT pulmonary angiograms for calculation of clot burden scores. With advances in technology, MDCT pulmonary angiographic clot burden scores may more accurately estimate the subsegmental pulmonary artery clot burden. That we did not use the current CT technologic advances limits the value of this study, although to our knowledge it is the largest prospective study published on this topic. Finally, no CT parameters for right heart failure or echocardiographic parameters for pulmonary hypertension were estimated in our study. In conclusion, we found a poor correlation between the ECG score and the CT pulmonary angiographic clot burden in our cohort of patients with pulmonary embolism. 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