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Clinical Observations |
1 Division of Thoracic Radiology, Massachusetts General Hospital, Founders 202,
55 Fruit St., Boston, MA 02114.
2 Division of Nuclear Medicine, Massachusetts General Hospital, Boston,
MA.
Received May 13, 2006;
accepted after revision December 29, 2006.
Address correspondence to C. Wittram
(cwittram{at}partners.org).
Abstract
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CONCLUSION. The activity of acute pulmonary embolism on FDG PET scans was significantly higher than the activity of vessels not containing thrombi. The shape of the abnormal FDG uptake may be focal or curvilinear.
Keywords: CT • nuclear medicine • oncology • PET • pulmonary embolism
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There is a sustained increase in utilization of 18F-FDG PET in the evaluation of patients with known or suspected malignancy in the thorax [6]. Integrated PET/CT scanners have the added advantage of high anatomic resolution and the ability to show tissue with increased glucose metabolism. In the literature, a series of three pathologically proven pulmonary infarcts exhibited an increase in FDG uptake [7], and there has been one case report [8] of FDG uptake by pulmonary emboli. The purpose of our study was to evaluate pulmonary emboli on FDG PET scans in a large series of patients.
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PET/CT Technique
An integrated PET/16-MDCT scanner (Sensation, Siemens Medical Solutions)
was used to acquire the images. The patients were given an injection of 15 mCi
of FDG. Forty-five minutes later, attenuation-correction unenhanced CT scans
were acquired from neck to pelvis at 2-mm slice thickness, 83 ± 31 (SD)
mA (range, 60-150 mA) at 120 kVp, and 0.5-second tube rotation time. The
imaging field of view was the widest rib-to-rib distance acquired during quiet
breathing. The PET images were acquired at 3.75-mm slice thickness and mean
full width at half maximum of 6 ± 0.7 (range, 5-7). For the final CT
scan, IV access was through an antecubital vein. An injection of 120 mL of
ioxilan 300 mg I/mL was given through a 20-gauge catheter at 2.5 mL/s. Images
were acquired with a collimation and reconstruction width of 2.00 mm,
0.5-second tube rotation time, and 195 ± 43 mA (range, 166-275 mA) at
140 kVp. Image acquisition was started 48 seconds after commencement of IV
administration of contrast medium, and patients were asked to take a small
breath in and hold it. CT images were acquired with a standard algorithm. For
this study, the chest component was analyzed.
Diagnostic Criteria for PE and Pulmonary Infarction
One of the investigators identified acute PE as an intraluminal filling
defect that had a sharp interface with intravascular contrast enhancement that
manifested as follows: Complete arterial occlusion with failure to opacify the
entire lumen, sometimes with enlargement of the artery in comparison with
pulmonary arteries of the same order of branching
[9-11];
a central arterial filling defect surrounded by intravascular contrast
enhancement [9]; and a
peripheral intraluminal filling defect at an acute angle to the arterial wall
[10,
11]. In all three types of
manifestation, the anatomic levels of the pulmonary emboli were categorized
and recorded as main, right or left, interlobar, lobar, segmental, or
subsegmental pulmonary artery.
Because FDG can be taken up in both lymphadenopathy and PE, it was important to differentiate these abnormalities on contrast-enhanced CT. Lymph nodes were recognized as being in an extravascular location, and PE was recognized as an intravascular filling defect that fulfilled the three aforementioned diagnostic criteria for PE. The diagnosis of pulmonary infarction was considered on CT when a region of ground-glass opacification or consolidation was identified in lung parenchyma distal to a vessel occluded by thrombus.
Evaluation of Systemic Veins in the Abdomen and Pelvis
The veins of the abdomen and pelvis were evaluated for adequacy of vascular
opacification on contrast-enhanced CT and for the presence of thrombus. If
thrombus was identified, the corresponding PET image was evaluated for the
presence or absence of increased FDG uptake.
Quantitative Evaluation
All images were viewed on a Reveal-MVS workstation (Mirada Solutions). The
program resampled the contrast-enhanced CT data to accord with PET slice
thickness. For each axial level of a study, three images were displayed: the
CT image viewed on mediastinal window (width, 350 H; level, 40 H), combined
PET/CT image, and PET image. Two radiologists, one with 10 years of experience
in thoracic radiology, and a nuclear medicine radiologist with 20 years of
experience in nuclear medicine interpretation reviewed the images at one
sitting. The largest thrombus in an individual lung was identified, and a
region of interest was drawn around the margin of the vessel. After input of
the patient's body weight, the maximum standard uptake value (SUV) from the
region of interest was recorded. A vessel of similar size, which did not
contain thrombus, also was identified. The process was repeated for this
vessel, and the data recorded. Region-of-interest measurements of vessels
containing and not containing thrombus were obtained from vessels that did not
have visually detectable lymphatic tissue or extravascular soft tissue around
the vessel. The cases with infarction were identified, an SUV region of
interest was drawn around the margin of the opacity, and the maximum SUV was
recorded. A normal region of lung on the opposite side with a similarly sized
region of interest was used as a control.
Qualitative Evaluation
All cases were reviewed by consensus to evaluate the shape of the abnormal
FDG uptake by pulmonary emboli. Six patients had undergone prior
contrast-enhanced CT and PET that did not show PE. In these six cases, the
study images and previous PET images were viewed side by side to evaluate for
interval change.
Statistical Analysis
The two-tailed paired Student's t test was used. Statistical
significance was considered when p < 0.05.
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All patients had evidence of acute PE on contrast-enhanced CT. No cases of chronic embolism were identified. The site of the largest pulmonary embolus was the right pulmonary artery in two cases, lobar artery in nine cases, and segmental artery in two cases. In two cases, no previous contrast-enhanced CT scans were available. In 11 cases, previous contrast-enhanced CT scans showed evidence of PE in four cases, less thrombus than visualized with PET/CT in three of the four cases, and a larger thrombus in one case. In the other seven cases, previous CT showed no evidence of PE. The mean time between previous CT and PET/CT was 11 ± 9 weeks (range, 2-28 weeks). Follow-up CT scans were available for eight of the study patients, and all scans showed the thrombus had cleared. The time period between the study CT and follow-up contrast-enhanced CT was a mean of 19 ± 12 weeks (range, 7-34 weeks).
All but one patient received anticoagulation therapy as a result of the diagnosis of coincidental PE. The other underwent placement of an inferior vena caval filter. The mean SUV of acute PE was 1.65 ± 0.61 (range, 0.45-3.03). Vessels without thrombus had a mean SUV of 1.15 ± 0.38 (range, 0.42-1.64) (p = 0.009). The average SUV per vessel size was the main pulmonary artery, 1.5 ± 0.27 (range, 1.3-1.69); lobar pulmonary artery, 1.75 ± 0.60 (range, 1.24-3.03); and segmental pulmonary artery, 1.57 ± 0.75 (range, 0.45-2.62). In three cases, CT showed lung opacification peripheral to the acute thrombus: consolidation in two of the cases and ground-glass opacification in one case. These lesions were consistent with infarction and had a mean SUV of 1.84 ± 0.96 (range, 0.8-2.69). The normal region of lung had a mean SUV of 0.80 ± 0.29 (range, 0.56-1.13) (p = 0.129).
In all six cases in which previous PET/CT had not shown PE, direct comparison of the study PET scans with the previous images showed evidence of an increase in FDG uptake in the hila. This increased uptake represented a new focal or curvilinear abnormality corresponding to the contrast-enhanced CT abnormality that represented PE (Figs. 1A, 1B, 1C, 1D, 2A, 2B, 2C, 2D, 2E, and 2F).
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Pulmonary infarction causing increased uptake of FDG has been described in three cases [7]. This study demonstrates that PE can also cause an increase in FDG uptake on PET scans. The differential diagnosis of vascular uptake of FDG in the thorax includes atheromatous disease, which is common in the systemic arteries [14], and Takayasu arteritis, which can affect both systemic and pulmonary arteries [15].
The pathologic mechanism of acute PE often involves impaction of thrombus within a pulmonary artery by pulsatile flow. Distention of an affected artery can lead to focal vessel wall inflammation and necrosis with aggregation of leukocytes along the endothelial surface. These changes can occur within the first few days of the onset of pulmonary thromboembolic disease. Vascular uptake of FDG in atheroma and Takayasu arteritis is caused by inflammation [14, 15]. It is assumed that a similar process is the cause of acute PE.
Although they are not yet clarified, the exact mechanisms of FDG uptake by PE are likely related to the chemical characteristics of the radiopharmaceutical. This glucose analogue has a biodistribution determined in large part by increased numbers of glucose transporter proteins and increased intracellular levels of hexokinase and phosphofructokinase, among other agents, which promote glycolysis. FDG is well known to be taken up by inflammatory cells [16]. The rationale is that activated macrophages and neutrophils in inflammatory tissue use glucose as an energy source for chemotaxis and phagocytosis, whereas fibroblasts use glucose for proliferation [17]. We hypothesize that a local increased influx of inflammatory cells causes a focal increase in uptake of FDG at the embolic site. Further study of the exact mechanism is required.
In a population of oncology patients, one concern for this study was how to differentiate thrombotic and tumor emboli as a cause of the intravascular filling defects. As a rule, large tumor emboli that affect vessels of segmental size or larger arise from tumors that invade the inferior vena cava or large feeding veins. Examples are hepatoma, renal cell carcinoma, and choriocarcinoma [18]. In our group of 13 patients, no patient fit this criterion. In addition, in cases in which follow-up contrast-enhanced CT scans were available, eight patients had complete resolution of PE after anticoagulation therapy.
One limitation of our study was the relatively small size of the population. More subjects would have been included if the search had incorporated cases in which FDG PET and contrast-enhanced CT were performed at different times. Use of this criterion, however, would likely have produced less accurate data because of a potential rapid change in size and position of emboli as a result of fragmentation and lysis. We chose fewer subjects and greater accuracy. Another limitation, as in all PET/CT studies, was that we assumed accurate registration of the CT and PET images. Despite this limitation, our results show the importance of temporal correlation, because an increase in FDG hilar uptake can indicate PE. An additional limitation was that only 13 (0.59%) of 2,216 patients with tumors were identified as having PE. This number is much lower than in other series described [3-5]. The explanation is that our cases were identified with a word-search system, which can miss cases of coincidental PE not reported by radiologists. The objective of this study was not to evaluate the rate of coincidental PE in a group of oncology patients but to describe the manifestations of FDG uptake by PE.
In conclusion, many patients undergo integrated PET/CT for tumor detection, staging, and evaluation for response to therapy. The presence of coincidental PE is likely in this population and should be recognized in the contrast-enhanced CT component of PET/CT studies. In patients who do not receive IV contrast material, a focal or curvilinear increase in FDG uptake over a vessel should suggest the possibility of PE, and further imaging with CT angiography should be considered.
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