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(Chest. 2006;129:192-197.)
© 2006 American College of Chest Physicians

Resolution of Thromboemboli in Patients With Acute Pulmonary Embolism*

A Systematic Review

Mathilde Nijkeuter, MD; Marcel M.C. Hovens, MD; Bruce L. Davidson, MD, MPH, FCCP and Menno V. Huisman, MD

* From the Department of General Internal Medicine and Endocrinology (Drs. Nijkeuter, Hovens, and Huisman), Leiden University Medical Centre, Leiden, the Netherlands; and Pulmonary and Critical Care (Dr. Davidson), Swedish Medical Center and University of Washington School of Medicine, Seattle, WA.

Correspondence to: Menno V. Huisman, MD, Department of General Internal Medicine and Endocrinology, Leiden University Medical Centre, C4 R68, Albinusdreef 2, 2333 ZA, Leiden, the Netherlands; e-mail: M.V.Huisman{at}lumc.nl

Abstract

Study objectives: Much attention has been paid in recent years to optimizing the diagnosis of acute pulmonary embolism (PE). However, little is known about the changes in clot burden that occur at the level of the pulmonary arteries after documented PE. It is often problematic to distinguish between a new or residual defect on lung scintigraphy or helical CT. This may lead to falsely labeling patients with residual PE as having recurrent PE and consequent unnecessary treatment changes.

Design: We performed a systematic analysis of studies of imaging tests (radionuclide and CT) evaluating resolution rate of PE with independent assessment of predefined methodologic criteria by two investigators.

Results: We identified 29 clinical studies. Of these, 25 studies were excluded and 4 studies were included in our review. Because studies differed largely in patient selection, duration of anticoagulation, and timing of follow-up, the studies were not pooled but briefly described. The percentage of patients with residual pulmonary thrombi was 87% at 8 days after diagnosis, 68% after 6 weeks, 65% after 3 months, 57% after 6 months, and 52% after 11 months.

Discussion: This review shows that complete resolution of PE is not routinely achieved between 8 days and 11 months after diagnosis. More than 50% of patients with PE still have defects 6 months after diagnosis, after which resolution of thrombi appears to reach a plateau phase. Physicians should be aware of the high percentage of incomplete resolution of pulmonary emboli. Routine re-imaging after cessation of anticoagulant therapy in patients with PE to obtain a new baseline could be considered.

Key Words: follow-up diagnostic studies • pulmonary embolism • residual thrombosis • resolution

Much attention has been paid in recent years to optimizing the diagnosis of acute pulmonary embolism (PE). Helical CT is increasingly preferred as a first-line test. However, little is known about the subsequent changes in clot burden that occur in pulmonary arteries after objectively documented PE. In patients with symptomatic objectively proven proximal deep vein thrombosis of the leg veins, studies12 of sequential ultrasound examinations have demonstrated that persistent residual thrombosis is common after treatment with short-term anticoagulation and, according to one report,3 "normalization" of the image is achieved in 39% at 6 months, 58% after 12 months, and 74% at 36 months, while other studies45 suggest other time ranges. Information regarding the rate of resolution of pulmonary thrombi after diagnosis of PE is important because it may facilitate objective diagnosis when patients with PE return with complaints possibly due to recurrent PE. It is often clinically difficult to determine whether defects suggesting pulmonary emboli on lung scintigraphy or helical CT are residual or represent a new event. In a prospective study,6 it has been shown that 4% of first-time, symptomatic PE patients acquire symptomatic chronic thromboembolic pulmonary hypertension (CTPH) within 2 years. It would be desirable to avoid this outcome if possible and likewise to prevent the cascade of treatment consequent to falsely labeling patients with a recurrent PE. To better understand the natural history of pulmonary artery clot evolution after objectively documented PE, we performed a systematic analysis of published studies addressing this important clinical problem.

Materials and Methods

Search Strategy
We used electronic search strategies to identify relevant studies. The following electronic databases were searched: PubMed (1966 to November 2004), EMBASE (1980 to November 2004), Cochrane, the Library Issue 1, 2005, and Web of Science using the following search terms: residual thrombosis or incomplete recovery or incomplete resolution or (resolving AND [clots OR clot]) or ([normalization OR normalization] AND [pulmonary arteries OR pulmonary artery]) or ([(thrombi AND regression) or thrombus regression] AND [pulmonary embolism OR pulmonary embolic OR [pulmonary AND (embolism OR emboli OR embolus)]) or (scintigraphic AND control AND pulmonary embolism). We augmented our search by reviewing the reference lists of retrieved articles. Studies published in any language were used.

Study Selection
We attempted to identify all published clinical studies that evaluated patients with PE and the rate of resolution of pulmonary emboli visualized by follow-up objective imaging tests. Of potential articles, abstracts were read to determine eligibility; in case of doubt, full-text articles were retrieved. To be included, a study had to have the following: (1) be prospective and involve consecutive patients; (2) objectively diagnose symptomatic PE (pulmonary angiography [PA] or helical CT, high-probability ventilation/perfusion [V/Q] lung scintigraphy, or intermediate-probability V/Q scan with positive compression ultrasonography or venography); (3) use objective imaging tests at follow-up; (4) describe the duration and type of treatment of PE with a minimum administration of anticoagulant therapy of 6 weeks and no allowance of vena cava ligation, femoral ligation, or pulmonary embolectomy; (5) identify whether there was a prior history of venous thromboembolism; and (6) provide a description of the method of follow-up.

Data Extraction
Two investigators independently assessed studies for inclusion according to the predefined methodologic criteria. Investigator disagreements were resolved by majority opinion of a third investigator. Study authors were contacted as required to retrieve missing information.

Results

We identified 29 clinical studies. Of these, 25 studies were excluded for the following reasons: (1) retrospective design789101112131415; (2) nonconsecutive patients7101112131617181920212223242526272829; (3) lack of objective verification of the diagnosis1017182130; (4) asymptomatic patients25; (5) treatment with inferior vena cava ligation or femoral ligation, embolectomy, or no treatment in some patients789101116181920212324252931; (6) anticoagulant therapy for < 6 weeks10182324; and (7) no description of history of venous thromboembolism.122829 The excluded studies and reason for exclusion are listed in Table 1 . Four studies32333435 remained for inclusion in our review of rate of resolution of thrombi in patients with PE (Table 2 ). Two studies2829 used V/Q lung scintigraphy as the follow-up test, and two studies3031 used helical CT. The included studies differ not only in objective diagnostic tests used at follow-up but also in duration of follow-up and duration of treatment. Therefore, we decided not to pool data statistically but to describe the studies briefly.


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  		Table 1.. Excluded Studies*

 

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  		Table 2.. Included Studies

 
Studies Using V/Q Scintigraphy at Follow-up
Hvid-Jacobsen et al32 re-examined 30 consecutive patients 6 months after diagnosis of PE. All patients were available for follow-up. All underwent repeat V/Q scans and chest radiographs, and all had been treated for 3 months. Six months after diagnosis, 13 patients (43%) had normalized scan findings, 9 patients (30%) had minor defects, 6 patients (20%) had persistent defects, and 2 patients had new defects. None of the patients had symptoms of recurrent PE. In this early study,32 the authors concluded that defects could not be assumed to have resolved 6 months after diagnosis of PE and that rescanning after treatment should be done to obtain a new baseline. A limitation of this study is the 3-month time interval between cessation of anticoagulant treatment and follow-up scan. The time course of natural resolution of pulmonary thrombi with anticoagulant therapy in this study may be confounded by the asymptomatic recurrence of PE in the 3-month period without treatment.

Wartski et al33 included 157 patients from the Tinzaparin ou Heparin Standard: Evaluation dans l’Embolie Pulmonaire Study, a multicenter, randomized, comparison of continuous, adjusted-dose IV heparin vs once-daily, subcutaneous, low-molecular-weight heparin followed by oral anticoagulants for 3 months in 612 patients with acute PE.3336 The results showed both initial therapies to be equally effective. The two treatment groups did not significantly differ in age, sex, weight, or percentage of vascular obstruction (PVO) and were therefore pooled. Of 157 patients at study entry, 145 patients had high-probability lung scans and 12 patients had intermediate lung scans with deep vein thrombosis confirmed by venography or compression ultrasonography. In all patients, routine follow-up perfusion lung scintigraphy was performed after 8 days and after 3 months with no loss to follow-up. The degree of PVO was calculated for each scan by assigning a weight to each lobe, based on regional blood flow distribution, and subsequently estimating a quantitative score from 0 (no perfusion) to 1 (normal perfusion) on the basis of {gamma} count defects seen in each lobe. Lobar perfusion score was calculated by multiplying the assigned weight of each lobe by the perfusion score. The overall score is the sum of the six separate lobar scores (the lingula is counted as a separate lobe), and PVO (percentage) is calculated as follows: (1 – total perfusion score) x 100%. Three months after diagnosis, 53 patients (34%) had normalized perfusion lung scans; 21 of these patients (13% of the total) had already normalized perfusion by day 8. Of the 157-patient cohort, 16 patients (10%) had no resolution of perfusion defects whatsoever after 3 months. An additional 28 patients (18%) of the total cohort had some improvement by day 8 but no further resolution by 3 months. These authors also concluded that follow-up scintigraphy serves as a new baseline for the diagnosis of recurrent PE.33 Furthermore, they suggest that a follow-up scan may help to identify patients who are likely to progress to CTPH on the basis of extensive residual defects.

Studies Using Helical CT at Follow-up
Remy-Jardin et al34 were among the first to use helical CT as a follow-up test to evaluate the resolution of acute PE. Of 111 eligible patients referred to an ICU with massive acute PE, 49 patients did not undergo follow-up evaluation for the following reasons: the patient died during follow-up (22 patients), the patient had a history of (extra-)thoracic malignancy and a poor clinical status (10 patients), the patient was > 85 years old (7 patients), the patient had a history of allergic reactions to contrast agent (2 patients), or the patient refused (8 patients). In the remaining 62 consecutive patients, a follow-up CT scan was performed a mean of 11 months after onset to analyze the outcome of endoluminal clots after at least 6 months of anticoagulation therapy. The diagnosis of acute PE was made with PA (n = 43) or helical CT (n = 19). Although main, lobar, and segmental arteries were evaluated, only data regarding the extent of PE (severity scores: minor PE, when < 25% obstruction; moderate PE, 26 to 50% obstruction; severe PE, at least 51% obstruction) and not the location of PE were provided. For 59 of the 62 patients, the massive acute PE was their first episode of thromboembolism; 3 of 62 patients had a history of chronic thromboembolic disease. Complete resolution of thrombi at a mean of 11 months (range, 1 to 53 months) was shown in 48% of patients, and endovascular abnormalities were present in 52%.30 Within this follow-up period, there were no clinical episodes of recurrent PE. Follow-up scans were categorized as showing resolution of thrombi (group 1) or endovascular abnormalities (group 2). Group 1 patients showed no cardiopulmonary symptoms or echocardiographic abnormalities, while 6 of 32 group 2 patients (9.7% overall) had dyspnea on exertion, and 5 group 2 patients (8.1% overall) had echocardiographic findings of pulmonary hypertension. Furthermore, group 2 patients were categorized as follows: (1) patients with partial resolution of initial thrombi (n = 24), and (2) patients with CT features of chronic PE, defined as severe arterial narrowing of > 50% of the arterial diameter developing between the time of the initial diagnosis and the posttherapeutic follow-up. A striking finding was that eight patients (13%) had CT signs of chronic PE over a median follow-up of 8.5 months (range, 2 to 30 months) despite an anticoagulant course of at least 6 months and no symptomatic recurrences. The authors34 conclude that helical CT might help in understanding changes within central pulmonary arteries after massive acute PE, enabling not only the in vivo surveillance of organized and recanalized clots but also of arterial narrowing (a sign of chronic PE) in asymptomatic patients.

Van Rossum et al35 described the helical CT appearance of clots 6 weeks after acute PE. Of 29 consecutive patients with confirmed PE, 9 patients refused a follow-up scan and 1 patient died of massive PE shortly after the diagnosis, leaving 19 patients for analysis. Clots on the initial and follow-up scan were classified into five categories: (1) central filling defect or complete occlusion (the established CT criteria for acute PE); (2) eccentric clot contiguous with the vessel wall at the site of acute PE on the initial scan; (3) filling defect with central contrast material indicating recanalization; (4) severe arterial luminal narrowing or vessel occlusion of a stenosed artery (the established criteria for chronic PE); and (5) normally enhancing vessels at follow-up indicating complete resolution of clots. At the initial CT scan, all patients (n = 19) had type 1 clots, a sign of acute PE. Normalization of pulmonary arteries at 6-week follow-up was seen in six patients (32%). Of the 13 patients (68%) with residual abnormalities, 2 patients still had solely type 1 clots. In the 11 remaining patients, most of the emboli had disappeared but some residual emboli were present as eccentric emboli contiguous with the vessel wall (22% of initial 153 clots) or filling defects with central contrast material (3% of initial 153 clots) representing recanalization (ie, type 2 and type 3 clots). In one of these patients, signs of chronic PE at the initial scan remained unchanged at follow-up. The authors of this study35 wondered whether existing CT criteria for chronic PE are as specific as assumed since this study showed that eccentric emboli contiguous with the vessel wall and evidence of recanalization are already present at the 6-week follow-up in 22% and 3% of clots, respectively. No vascular narrowing or stenosis with occlusion was found, which may be more specific criteria for chronic PE. Figure 1 summarizes our findings regarding the percentage of patients with residual thrombi in patients who presented with acute PE in the four studies described.


Figure 1
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  		Figure 1.. Included studies: {diamondsuit}, Wartski and Collignon33; •, van Rossum et al35; {blacksquare}, Hvid-Jacobsen et al32; and {blacktriangleup}, Remy-Jardin et al.34

 
Discussion

This review shows that complete resolution of pulmonary thromboembolism is not routinely achieved between 8 days and 11 months after acute PE. Overall, > 50% of patients with PE have persistent defects at their follow-up scan 6 months after diagnosis (Fig 1). Afterward, resolution of thrombi seems to reach a plateau phase, since complete resolution is found in 43% of patients after 6 months and in nearly the same percentage of patients (48%) after 11 months. Of interest is the wide variation in resolution of thrombi in individual patients. Complete resolution of pulmonary thrombi was already present in 13% of patients 8 days after diagnosis of PE, while in 10% of patients no change in thrombotic occlusion was seen after 3 months. The pathophysiologic mechanisms of resolution of thrombi and the risk factors and clinical consequences of partial resolution remain largely unknown.

There are several methodologic issues within the included studies in our review. First, the timing of follow-up was not standardized between the studies, varying from 8 days to 6 months. In the study of Remy-Jardin et al,34 there was no prespecified timing of follow-up, and hence follow-up ranged from 1 to 53 months. Similarly, the duration of anticoagulation therapy differed in length and in timing related to the follow-up scan, varying from 6 weeks to > 6 months. Also, there is no current standard technique for imaging resolution of PE. Two studies3233 used V/Q scintigraphy, and two studies3435 used CT scan as a follow-up diagnostic method, but it is apparent that these two techniques are not interchangeable. Perfusion scintigraphy is a functional test but is reported to underestimate the presence of thromboembolic disease and also the severity of angiographic and hemodynamic compromise in CTPH.3334 Helical CT depicts the morphology of the pulmonary arteries but contains no information regarding pulmonary functional status. Moreover, no uniform criteria are used in defining chronic imaging defects, even when similar imaging methods were used. In view of the included study of Remy-Jardin et al,34 for which the CT technology was only capable of imaging central pulmonary arteries, our findings may not apply to smaller pulmonary emboli, either symptomatic or incidentally discovered. Last, a confounding but unavoidable fact in prior or future studies is that for patients with a first PE, it cannot be confidently ruled out that imaging defects were already present before the diagnosis, since the majority of patients have no scan before their first thromboembolic event. With radionuclide scans, physicians cannot be certain, even with the aid of concomitant chest CT scans, that persistent defects represent residual thrombi rather than other defects responsible for decreased perfusion.

What are the implications of our findings for the future management of PE? First, physicians should be aware that complete resolution of pulmonary thrombi is not achieved in > 50% of patients 6 months after diagnosis of PE and that this fact may complicate the objective and accurate diagnosis of recurrent PE. Second, an attempt should be made to generate an international consensus among physicians caring for PE patients, including radiologists and nuclear medicine physicians, regarding the optimal way of imaging, interpreting, and reporting of resolution of pulmonary emboli and diagnosing chronic PE. Third, routine re-imaging after cessation of anticoagulant therapy in patients with PE to obtain a new baseline could be considered.35 The timing of such a follow-up scan as a new baseline test is likely to be most valuable at the time considered for cessation of anticoagulant therapy. Finally, in patients with persisting thromboembolic obstruction or with persisting cardiopulmonary complaints, one should be alert for chronic PE and the development of CTPH.2

In conclusion, resolution of pulmonary thrombi is not routinely achieved after acute PE. The pathophysiologic mechanisms, risk factors, and clinical implications of incomplete resolution are not well established. There is a clear need for prospective well-designed follow-up studies to more accurately define the resolution rate after documented PE and related prognostic factors.

Footnotes

Abbreviations: CTPH = chronic thromboembolic pulmonary hypertension; PA = pulmonary angiography; PE = pulmonary embolism; PVO = percentage vascular obstruction; V/Q = ventilation/perfusion

Received for publication May 31, 2005. Accepted for publication August 5, 2005.

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