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Nuclear Medicine |
1 From the Russell H. Morgan Department of Radiology and Radiological Science, Division of Nuclear Medicine, Johns Hopkins Medical Institutions, 601 N Caroline St, Rm 3223A, Baltimore, MD 21287-0817. Received September 13, 2002; revision requested November 20; final revision received May 15, 2003; accepted May 20. Address correspondence to R.L.W. (e-mail: rwahl@jhmi.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Records of 85 consecutive cancer patients who underwent FDG PET/CT were evaluated retrospectively. One hour after FDG injection, CT followed by PET was performed from ear to middle of the thigh. CT, PET, and fused PET/CT images were generated. FDG uptake and calcification were evaluated visually and semiquantitatively. FDG uptake was graded according to intensity; calcification, according to thickness. Unpaired t test was used for comparison of patient age with and without FDG uptake and with and without calcification. The relationship between the score (sum of grades along all aortic segments) of positive FDG uptake and calcification and patient age was analyzed with Spearman rank correlation. Comparison of frequency of FDG uptake and calcification with age, sex, risk factors for cardiovascular disease (CVD), or history of CVD was performed with 
2 analysis.
RESULTS: Fifty patients had at least one area of FDG uptake in thoracic aortic wall, 14 of whom showed focal FDG uptake. Intermediate to intense FDG uptake tended to be observed in the descending aorta. Forty-five patients had at least one measurable aortic calcification. Thick calcification was observed most often at the aortic arch. Twelve patients had 13 uptake areas at the calcification site. Patients with positive findings were on average older (P < .05 for both increased uptake and calcification); the older patient group had higher frequency of both aortic wall uptake (P < .005) and calcification (P < .001). The calcification score correlated with age (
= 0.60, P < .001) but the FDG uptake score did not. Women, patients with hyperlipidemia, and patients with history of CVD tended to show increased FDG uptake (P = .073, .080, and .068, respectively), whereas patients with diabetes had significantly more calcifications (P < .05).
CONCLUSION: PET/CT depicted FDG uptake commonly in the thoracic aortic wall. The FDG uptake site was mostly distinct from the calcification site and may possibly be located in areas of metabolic activity of atherosclerotic changes.
© RSNA, 2003
Index terms: Aorta, CT, 56.12111, 94.12911 • Aorta, diseases, 56.754 • Arteries, calcification, 56.812 • Dual-modality imaging, PET/CT • Images, fusion • Positron emission tomography (PET), 56.12163, 94.12963
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Positron emission tomography (PET) with the glucose analog fluorine 18 (18F) fluorodeoxyglucose (FDG) is increasingly recognized as a valuable molecular imaging method. 18F FDG (hereafter, FDG) PET enables detection of the increased glucose metabolic rate that is characteristic of most cancers and has been shown to be useful for initial tumor diagnosis and staging, for detection of tumor recurrence, and for evaluation of the response to chemotherapy or chemotherapy and radiation therapy of various kinds of malignant tumors (7–10). The brain has a high level of glucose metabolism, and many nonmalignant processes such as infection and inflammation also have increased glucose metabolism. It is possible that glycolytic metabolism is increased in the inflammatory component of active atherosclerotic change in arteries. We have shown in experimental atherosclerosis that there is a markedly increased FDG uptake, which can be detected with direct examination of the vessel with a radiation-sensitive probe (11). Increased FDG uptake in the region of the aorta has been reported in human studies, but to date there is little information regarding its frequency, location, or intensity (12–14). In the carotid arteries, FDG PET has been suggested to allow detection of active atherosclerotic plaques and differentiation of symptomatic or unstable plaques from asymptomatic lesions (15).
Recently, a combined PET/computed tomography (CT) has emerged as a promising imaging modality and is now beginning to be used more routinely in clinical situations (16–18). PET/CT imaging allows routine and precise fusion of metabolic PET images with high-quality CT images. The exact location of FDG uptake can be determined with these PET/CT images. Thus, the purpose of our study was to evaluate the presence, location, and intensity of FDG uptake in the thoracic aortic wall by using a combined PET/CT imaging device and compare the FDG uptake with the aortic wall calcification.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patients
Eighty-five consecutive patients having undergone clinical FDG PET/CT studies, who were known to have or were suspected of having malignant tumors, were evaluated retrospectively. There were 46 male and 39 female patients (age range, 11–81 years; mean age, 55 years ± 16 [SD]). Eighteen patients underwent chemotherapy within a year before the PET/CT study. Seven patients underwent radiation therapy involving the aorta in the year before the PET/CT study. Their body weights ranged from 32.7 to 138.0 kg (mean, 73.6 kg ± 18.8). Nine patients had diabetes, and 25 patients were considered obese because their body mass index, or BMI, was equal to or more than 30, which is determined by dividing the person’s weight in kilograms by the square of the person’s height in meters (19). Information regarding diabetes and obesity was available for all of the 85 patients.
For 67 of the 85 patients, information was available regarding smoking, hypertension, and hyperlipidemia (hypercholesterolemia or hypertriglyceridemia), as well as history of cardiovascular disease (CVD), such as coronary artery disease. There were 17 active smokers, 15 patients with hypertension, 13 patients with hyperlipidemia, and 16 patients with CVD.
PET/CT Imaging
Whole-body FDG PET/CT imaging (Discovery LS; GE Medical Systems, Milwaukee, Wis) was performed. This imaging device allows the simultaneous acquisition of 35 transaxial images with an intersection spacing of 4.25 mm in one bed position for the PET images. Typically, six or more bed positions are obtained. Axial and transaxial image resolution is approximately 4.5-mm full width at half maximum. The field of view and pixel size of the reconstructed images are 50 cm and 3.91 mm, respectively. The system sensitivity is 200,000 cps/µCi. This imaging device also allows multi–detector row helical CT imaging.
The technical parameters used for the CT portion of the PET/CT imaging were as follows: a detector row configuration of 4 x 5 mm, pitch of 6:1 (high-speed mode), gantry rotation time of 0.8 second, table speed of 30 mm per gantry rotation, 140 kVp, and 80 mA. After at least 4 hours of fasting, adult patients received an intravenous injection of approximately 555 MBq (15 mCi) of FDG. About 60 minutes later, CT images were acquired from the meatus of the ear to the middle of the thigh for 37 seconds without contrast media. A whole-body emission PET scan for the same transverse coverage was then obtained, with a 5-minute acquisition per each bed position. Attenuation-corrected PET images were reconstructed with iterative reconstruction ordered-subset expectation maximization algorithm. The 5-mm-thick transaxial CT images were reconstructed at 4.25-mm intervals (transaxial) to fuse with the transaxial PET images. CT, PET, and fused PET/CT images (transaxial, coronal, and sagittal) were generated on a computer workstation for review and were reviewed together for each patient. Non–attenuation-corrected PET images were also reviewed.
Evaluation of the Aortic Wall
For the analysis of the thoracic aortic wall, images of the thoracic aorta were divided into three segments (ascending, arch, and descending), and the descending aorta was further divided into three equal segments (upper, middle, and lower) on the basis of the PET/CT images.
Abnormal FDG uptake in the thoracic aortic wall was evaluated visually on attenuation-corrected PET and PET/CT images, with consensus of two nuclear medicine physicians (M.T., C.C.), and was graded according to its intensity on PET images as follows: grade 1, slightly higher than blood pool and mediastinal uptake; grade 2, clearly shown and greater than grade 1 uptake but lower than liver uptake; and grade 3, equal to or greater than liver uptake. The longitudinal spread of the abnormal FDG uptake was recorded either as focal, linear, or bandlike according to the shape on coronal PET images. Semiquantitative analysis of the positive uptake (upake 
grade 1) was also performed by calculating the standardized uptake value corrected for lean body mass, or SUL, which is decay-corrected tissue activity divided by the ratio of the injected dose over the ideal body weight (20). The ideal body weight (IBW, in kilograms) can be calculated as follows: for men, IBW = 48.0 + (1.06 x [h - 152]) and for women, 45.5 + (0.91 x [h - 152]), where h is height in centimeters. The actual weight was used if the ideal body weight was greater than the actual weight (21). A region of interest was placed manually (M.T.) on the transaxial image to totally surround the most intense area of the FDG uptake, and the SUL was calculated by using the maximum pixel activity value within the region of interest. The size of the regions of interest ranged from 18 to 30 pixels (2.75–4.58 cm2). If multiple abnormal areas of FDG uptake were seen in one aortic segment and if they were each clearly distinguishable from one another, they were recorded separately.
Calcification in the aortic wall was evaluated (M.T., C.C., in consensus) by using 512 x 512-pixel CT images. If calcification existed, the greatest protrusion into the lumen from the aortic wall was measured (M.T.) on a transaxial image. Multiple calcifications in one aortic segment were also recorded in a manner similar to that used for the multiple areas of FDG uptake. Calcification was also graded as follows, according to its thickness: grade 1, less than or equal to 4 mm; grade 2, more than 4 mm or less than or equal to 8 mm; and grade 3, more than 8 mm. Although the extent of calcification could be measured in Hounsfield units, we graded calcifications according to thickness because this was viewed as more indicative of the total calcified vascular plaque burden.
To estimate the FDG uptake and calcification burden in the whole thoracic aorta in each patient, we defined a "score" as the sum of the grades of FDG uptake or calcification along all five aortic segments. This scoring system did not represent the actual amount of FDG uptake or calcification in the whole thoracic aortic wall but allowed classification of the patient’s aortic wall status based on the combination of the grade and the number of positive sites.
Patients were assigned into the following four groups according to the presence of FDG uptake and calcification: group A, patients without FDG uptake and without calcification; group B, patients only with FDG uptake; group C, patients only with calcification; and group D, patients with both FDG uptake and calcification.
Statistical Analysis
Data were expressed as mean ± SD. The unpaired t test was used for the comparison of patient age with and without FDG uptake and with and without calcification. For the comparison of patient age among the four groups based on FDG uptake and calcification, analysis of variance was performed followed by the post hoc Fisher test. The relationship between the highest intensity of FDG uptake or the size of the largest calcification in each patient and age was evaluated with a linear regression analysis. The relationship between the number or score of positive FDG uptake and calcification sites and patient age was analyzed with a Spearman rank correlation test. Comparison of the frequency of positive FDG uptake and calcification with age, sex, chemotherapy and/or radiation therapy within a year before the PET/CT studies, five risk factors (diabetes, obesity, smoking, hypertension, and hyperlipidemia) for CVD, or history of CVD was performed with a 2 analysis. P < .05 was considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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= 0.47, P < .005; and = 0.60, P < .001, respectively) (calcification score, Fig 5b). On the basis of the presence of FDG uptake and calcification among the four groups, patients in group A were the youngest (38 years ± 22; P < .05 vs group B, P < .01 vs groups C and D), followed by those in group B (49 years ± 7; P = .080 vs group C, P < .01 vs group D), those in group C (59 years ± 12), and those in group D (64 years ± 12). Women tended to have a higher frequency of positive FDG uptake than did men (P = .073), but this was not true of calcification (P = .47) (Table).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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FDG uptake in the thoracic aortic wall was observed in 50 of 85 consecutive patients in this study. This frequency is high but consistent with that in prior reports (13,14). However, this high frequency reduces the possibility that all of the aortic wall FDG uptake observed in this study corresponded to the atherosclerotic changes that led to serious cardiovascular events. Active atherosclerotic changes likely have been detected, but to establish PET findings of atherosclerotic changes at high risk of rupture, further studies are required in which positive FDG uptake is compared with histopathologic or other imaging results. The frequency of the aortic wall FDG uptake was higher in older patients than in the younger patients. Interestingly, neither the intensity, the number of positive sites, nor the score of positive FDG uptake in the whole thoracic aorta in each patient correlated with age. By contrast, the size of the largest deposit, the number of positive sites, and the score of positive calcification in each patient were all positively correlated with age. Moreover, most of the FDG uptake sites were not accompanied by calcification, and each of the FDG sites was separate from the nearest calcification site (if any). These results clearly demonstrate that the FDG uptake sites had significantly different characteristics than the aortic calcification sites and that most of the calcification sites had no or little cellular activity. It may be possible that FDG-avid vascular changes are precursor lesions, eventually followed by calcification at the same site. If so, there could be a substantial time lag between the precursor lesions and calcification.
The frequency of the aortic wall FDG uptake tended to be higher in women than in men and in patients with hyperlipidemia. Atherosclerosis has been shown to progress rapidly after menopause (24,25). Most (72%, or 28 of 39) of the female patients in this study were older than 50 years; thus, aortic wall FDG uptake may have included early active atherosclerotic lesions. Calcification frequency was comparable between men and women. Plasma lipids are known to be associated with plaque formation; thus, hyperlipidemia has a close relationship with atherosclerosis. Ross (4) reported that although atherosclerosis does not result simply from the accumulation of lipids but from the inflammatory process, hypercholesterolemia is a major factor in plaque formation. The fact that hyperlipidemic rabbits with arterial injury are often used as an experimental plaque model supports this relationship (11,22,23). In our study, calcification did not have a relationship with hyperlipidemia. These indirect data may support the hypothesis that FDG accumulates in areas of atherosclerosis, quite possibly earlier atherosclerotic lesions that antedate calcifications. However, further evaluation in a larger number of patients is obviously necessary to prove this hypothesis. According to the recent report of 192 patients, obesity and hyperlipidemia significantly related to the aortic wall FDG uptake (14).
Thoracic aortic wall calcification was observed in 45 (53%) of the 85 the patients in this study. The site of calcification had different characteristics from the site of FDG uptake. The size of the largest deposit, the number of positive sites, and the extent of the burden of calcification in each patient correlated with age, and calcification tended to be associated with history of CVD in this study. Aortic calcification is thought to reflect the systemic extent of atherosclerosis and to be a marker of CVD at a subclinical stage. Aortic and coronary calcification is an important prognostic indicator. Authors of a clinical study (26) reported that aortic arch calcification was independently related to coronary artery disease risk in both men and women, as well as to the risk of stroke in women. Authors of another large study (27) in which x rays were used reported that abdominal aortic calcification was a marker of subclinical atherosclerosis and an independent predictor of subsequent vascular morbidity and mortality. The advent of multi–detector row helical CT allows whole-body imaging with thin sections in a short time and, therefore, detection of calcification without difficulty. FDG PET/CT imaging is a potentially powerful tool for the evaluation of atherosclerotic status from two different viewpoints, provided that the aortic wall FDG uptake is also a marker of atherosclerotic changes.
In the present study, we assigned patients into four groups according to the presence of aortic wall FDG uptake and calcification. Although the number of patients in each group was small, patients with neither FDG uptake nor calcification were younger than patients with either FDG uptake or calcification, and patients with FDG uptake alone were younger than those with both FDG uptake and calcification. Moreover, patients with either of the risk factors for CVD showed a higher frequency of positive FDG uptake and calcification compared with patients without these risk factors. Patients with a history of CVD tended to have positive FDG uptake or calcification. These results suggest that FDG PET/CT imaging warrants further study of the risk stratification in patients with possible cardiovascular events. FDG PET/CT imaging could potentially be beneficial to patients with abnormal findings, if early lesion detection leads to effective prevention or reversal of atherosclerotic disease and avoidance of future serious complications. Further studies in a different population of patients are clearly required to test this hypothesis. Although we did not have histopathologic results, aortic wall FDG uptake may be located in areas of metabolic activity of atherosclerotic changes. In this regard, comparison of FDG PET/CT findings with C-reactive protein values may be of interest (28).
There are several possibilities other than atherosclerotic changes regarding aortic wall FDG uptake. First, the possibility of the reconstruction artifact being caused by using the CT attenuation correction method should be considered. The aortic wall exists as an interface between soft tissue and air or bone, where the reconstruction artifact occurs. However, aortic wall FDG uptake was also observed in the non–attenuation-corrected images in this study. Other investigators reported FDG uptake in the region of the aorta in germanium- or non–attenuation-corrected images (12,13). These images demonstrated that the aortic wall FDG uptake does not seem to be the artifact caused by the CT attenuation correction method. It should be noted, however, that the intensity of FDG uptake in the calcified region is potentially increased by using the CT attenuation correction method (29). While slight overestimation of the FDG uptake grade may have occurred, most of the calcification sites showed no increased FDG uptake in this study. The possibilities of false-positive findings of FDG uptake caused by other artifacts, such as a respiratory motion artifact, are improbable as non–attenuation-corrected images also showed aortic FDG uptake. However, artifacts from unknown causes may have increased the percentage of positive FDG findings. Media smooth muscle cells stressed by increased tension in the aortic wall may contribute to the FDG uptake. The aorta is, however, an elastic artery whose media consists of muscle cells and elastic fibers, in contrast to a muscular artery whose media consists only of muscle cells. Moreover, the media smooth muscle is considered to exhibit relatively low FDG uptake because the stress in the aortic wall is rather mild and continuous. The fact that the aortic wall FDG uptake was observed more frequently in older than younger patients may also decrease this possibility, since the vessels in the former tend to be rigid. No patients in this study had clinically diagnosed vasculitis at the time of FDG PET/CT studies, which might exhibit the aortic wall uptake. Although all patients had or were suspected of having cancer in this study, no data have been reported that cancer-related factors alter FDG uptake in the large arteries, which are separate from the cancers. Similarly, neither chemotherapy nor radiation therapy was related to FDG uptake in the aortic wall in this study.
FDG PET/CT is a recent modality for use in vascular disease imaging. In this study, CT was performed without contrast media, and we were thus unable to directly evaluate aortic wall changes such as wall thickening. With intravenous contrast enhancement and technical parameters better suited for CT imaging, improved vascular anatomic detail would be expected. Although in this study we did not compare PET results with the standards of histologic examination or outcome, and we are as yet unable to firmly clarify the clinical importance of the aortic wall FDG uptake, we believe that findings of this study illustrate the potential of molecular vascular imaging with FDG PET/CT.
In conclusion, FDG PET/CT imaging demonstrated that FDG uptake commonly occurs in the aortic wall. The tracer uptake site was mostly distinct from the location of the site of calcifications. The frequency of FDG uptake was significantly higher in patients 55 years or older and tended to be higher in women, patients with hyperlipidemia, and patients with a history of CVD. We raise the possibility that FDG PET/CT may be depicting the metabolic activity of atherosclerotic changes, which thus warrants, in our opinion, further study of the risk stratification in patients at risk of future cardiovascular events.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, R.L.W.; study concepts, M.T., R.L.W.; study design, all authors; literature research, M.T., R.L.W.; clinical studies, C.C., R.L.W.; data acquisition, C.C., R.L.W.; data analysis/interpretation, all authors; statistical analysis, M.T., Y.N.; manuscript preparation and editing, M.T., R.L.W.; manuscript definition of intellectual content and final version approval, R.L.W.; manuscript revision/review, all authors
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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