European Heart Journal

European Heart Journal Advance Access originally published online on August 5, 2007
European Heart Journal 2007 28(18):2243-2248; doi:10.1093/eurheartj/ehm245

This Article Abstract FREE Full Text (PDF) All Versions of this Article: 28/18/2243    most recent ehm245v1 E-letters: Submit a response Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (1) Request Permissions Disclaimer Google Scholar Articles by Tahara, N. Articles by Imaizumi, T. Search for Related Content PubMed PubMed Citation Articles by Tahara, N. Articles by Imaizumi, T. Social Bookmarking          What's this?

© The European Society of Cardiology 2007. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

The prevalence of inflammation in carotid atherosclerosis: analysis with fluorodeoxyglucose–positron emission tomography

Nobuhiro Tahara¹, Hisashi Kai^1,*, Hiroyuki Nakaura¹, Minori Mizoguchi¹, Masatoshi Ishibashi², Hayato Kaida², Kenkichi Baba², Naofumi Hayabuchi² and Tsutomu Imaizumi¹

¹ Department of Internal Medicine, Division of Cardiovascular Medicine, Cardiovascular Research Institute, Kurume University School of Medicine, 67 Asahimachi, Kurume, Fukuoka 830-0011, Japan
² Department of Radiology, Kurume University School of Medicine, Kurume, Japan

Received 19 February 2007; revised 25 April 2007; accepted 18 May 2007; online publish-ahead-of-print 5 August 2007.

^* Corresponding author. Tel: +81 942 31 7562; fax: +81 942 33 6509. E-mail address: naikai{at}med.kurume-u.ac.jp

	Abstract

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 
Aims: There is increasing evidence that ¹⁸F-fluorodeoxyglucose (FDG)–positron emission tomography (PET) imaging can be useful for non-invasive measurement of atherosclerotic plaque inflammation in humans. However, it is unknown how often atherosclerosis has inflammation in humans. Thus, we examined the prevalence of inflammation in documented carotid atherosclerosis using FDG–PET imaging.

Methods and results: FDG–PET imaging was performed in 100 consecutive patients who underwent carotid artery ultrasonography (CA-US) for screening of carotid atherosclerosis. Carotid atherosclerosis was considered when patients had the plaque score 5 and/or the focal thickening of the maximum intima-media complex 2 mm (localized plaque) by CA-US. The inflammation of carotid atherosclerosis was quantified by measuring the standardized uptake value (SUV) of FDG of the carotid artery. Inflammation was defined as present if the SUV score was 1.60 (1xstandard deviation above the average). FDG–PET imaging revealed inflammation in 12 of 41 (29%) patients having carotid atherosclerosis, whereas in 6 of 59 (10%) patients not having carotid atherosclerosis (P < 0.01). In patients with documented atherosclerosis by CA-US, body mass index, waist circumference, and the number of localized plaques were greater in a subset with inflammation than in a subset without.

Conclusion: Inflammation was visualized by FDG–PET imaging in 30% of patients with documented carotid atherosclerosis.

Key Words: Inflammation • Atherosclerosis • Carotid artery • Imaging

	Introduction

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 
Inflammation is highlighted in the pathogenesis and destabilization of atherosclerotic lesions.^1–4 Non-invasive identification of inflammation of atherosclerosis has been challenging. Circulating inflammation markers, such as high-sensitivity C-reactive protein, are useful for evaluating systemic inflammation and a risk stratification for cardiovascular diseases,^5,6 but not for the identification of inflammation of individual local lesions. Among the non-invasive imaging methods, high-resolution carotid artery ultrasonography (CA-US) is one of the best modalities for evaluation of morphology of atherosclerosis of the extracranial carotid arteries.^7,8 However, CA-US provides no information regarding inflammation of atherosclerosis.

Blockmans et al.⁹ reported that ¹⁸F-fluorodeoxyglucose (FDG)–positron emission tomography (PET) imaging was useful to detect large vessel vasculitis. Thereafter, several investigators demonstrated that FDG–PET imaging visualizes FDG uptake in human aorta and ilio-femoral artery even when there were no apparent symptoms or signs of vasculitis. The prevalence of FDG uptake was reported to be 50–60%.^10–12 However, in these previous studies, the reported prevalence was for the vessels of patients who underwent FDG–PET imaging mainly for cancer screening. Thus, the prevalence of FDG uptake is not known for atherosclerotic vessels. Recent studies have demonstrated that PET imaging co-registered with contrast-enhanced computed tomography (CT) or magnetic resonance imaging (MRI) visualizes FDG uptake in human carotid plaques and that the FDG accumulation is associated with macrophage infiltration in the excised plaques.^13–15 Towakol et al.¹⁵ have shown that carotid plaque FDG uptake is strongly correlated with macrophage density, a histological indicator of vascular inflammation,¹⁶ in the corresponding sections taken during carotid endarterectomy. Most recently, we have shown that statin therapy reduces FDG uptakes in human aorta and carotid artery.¹⁷ These observations suggest that FDG–PET imaging can non-invasively identify and quantify inflammation of atherosclerotic plaques, especially macrophage-related vascular inflammation. However, these studies did not address the prevalence of the FDG uptake in carotid plaques. Thus, the prevalence of inflammation in documented carotid atherosclerosis remained unknown. Accordingly, in the present study, we first documented the presence of atherosclerosis by CA-US and then investigated the prevalence of inflammation in carotid atherosclerosis by FDG–PET imaging. The present study has demonstrated for the first time that inflammation is visualized by FDG–PET/CT imaging in 30% of the patients who have documented carotid atherosclerosis but not having the history of recent ischaemic cerebrovascular disease (CVD).

	Methods

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 
Patient group
The study protocol was approved by the Ethics Committee for the clinical research of Kurume University for medical sciences. The study design was prospective. This study enrolled 100 consecutive patients (63±10 years, range 39–80 years; 64 males, 36 females) who underwent screening of carotid atherosclerosis by CA-US and then FDG–PET imaging at Kurume University Hospital. All patients gave written informed consent. This study excluded patients with (i) aortitis or vasculitis, (ii) active inflammatory diseases, (iii) acute coronary syndromes, (iv) uncontrolled diabetes mellitus or insulin treatment for diabetes mellitus, and (v) cancers. Also, patients on statin therapy were excluded, because our recent study has shown that statin attenuates plaque inflammation detected by FDG–PET imaging.¹⁷

Clinical and laboratory data
A questionnaire was administered to evaluate medical history, smoking habit, and drug use. After overnight fasting, peripheral blood was taken from the antecubital vein and subjected to measurements of lipid profile, fasting plasma glucose, hemoglobin A1c, fasting immunoreactive insulin, creatinine, and high-sensitivity C-reactive protein at a commercially available laboratory (Kyodo Igaku Laboratory, Fukuoka, Japan). The homeostasis model assessment of insulin resistance (HOMA-IR) was calculated using the following formula: HOMA-IR = fasting immunoreactive insulin (µU/mL)xfasting plasma glucose (mg/dL)/405. Creatinine clearance was computed with the Cockcroft–Gault equation.¹⁸

Hypertension was defined by the presence of systolic blood pressure 140 mmHg and/or diastolic blood pressure 90 mmHg or by taking prescribed antihypertensive medications. Hypercholesterolemia was diagnosed when low-density lipoprotein-cholesterol (LDL-C) was 140 mg/dL. Low high-density lipoprotein (HDL) cholesterolemia was defined if HDL-C was <40 mg/dL. Hypertriglyceridemia was defined if triglyceride was 150 mg/dL. Diabetes mellitus was defined by the presence of fast plasma glucose 126 mg/dL and/or hemoglobin A1c 6.4% or by having oral antidiabetics. History of ischaemic CVD includes major strokes and transient ischaemic attacks. All the 12 patients having CVD history did not experience CVD events for the last 12 months.

High-resolution B-mode ultrasonography
Carotid artery ultrasonography was performed with a high-resolution B-mode ultrasonography (Sonolayer SSA-380A, Toshiba, Tokyo, Japan) equipped with a 10 MHz transducer (PLF-703ST, Toshiba) by a technician blinded to other clinical information. The severity of carotid atherosclerosis was assessed by a scoring system proposed by Handa et al.^19,20 Briefly, the regions between 40 mm caudal from the beginning of the bifurcation bulb and 15 mm cranial from the flow divider of bilateral common and internal carotid arteries were scanned. All measurements were made at the time of scanning with the instrument's electronic caliper and were recorded on photocopies. The thickness of the intima-media complex (IMT) was measured as described by Pignoli et al.²¹ The plaque score was determined by summing measurements of the focal IMT of all localized thickenings in both carotid arteries.^19,20 And, when plaque score was 5 and/or the focal IMT was 2 mm (localized plaque), the patients were considered as having carotid atherosclerosis.

Fluorodeoxyglucose–positron emission tomography imaging
After at least 12 h of fasting, the study patients received an intravenous administration of 4.2 MBq (0.12 mCi) of FDG per kg body weight. One hour after an FDG injection, three-dimensional whole-body PET imaging was carried out using a PET scanner (Allegro, Philips Electronics, Tokyo, Japan). Contrast-enhanced CT images were also taken from the skull base to the diaphragm using Light Speed Ultra 16 (GE Yokogawa Medical System). The co-registration of PET and CT imaging (PET/CT imaging) was performed for review on a workstation (Sun Blade 2000, Sun Microsystem), as described previously.¹³ One representative case is shown in Figure 1. It is apparent that FDG uptake is located within the thickened vessel wall, i.e. atherosclerotic plaque. The intensity of FDG uptake was quantified by measuring the standardized uptake value (SUV) corrected for body weight. The SUV was calculated using the maximum pixel activity value within the region of interest placed on the vascular wall of the transaxial PET/CT image of the common carotid artery. The SUV score was determined as the average of the SUVs of both common carotid arteries obtained from 10 consecutive PET/CT images, each separated by 4 mm in length with the most cranial site starting at the carotid bifurcation. Two blinded radiologists measured the SUV, and the measurements were averaged. The intra- or inter-observer variability of SUV measurements was <5%. Inflammation was defined as positive when patients had the SUV score 1.60 (+1xSD above the average of 1.39±0.21 in the study patients).

View larger version (46K): [in this window] [in a new window] [Download PowerPoint slide]   Figure 1 Representative transaxial images of 18F-fluorodeoxyglucose–positron emission tomography, contrast-enhanced computed tomography, and their co-registration images showing 18F-fluorodeoxyglucose uptakes in the carotid artery. Black arrowhead denotes thickened vessel wall or atherosclerotic plaque. White arrowhead indicates vascular 18F-fluorodeoxyglucose uptake or inflammation. Physiological 18F-fluorodeoxyglucose uptakes are detected in the spinal cord (yellow arrow), the sternocleidomastoid muscle (green arrow), and the salivary glands (blue arrows).

 

	Results

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 
Inflammation of carotid atherosclerosis
Carotid artery ultrasonography demonstrated that 41 of 100 study patients had carotid atherosclerosis. PET/CT imaging revealed inflammation in 12 of 41 patients having carotid atherosclerosis [atherosclerosis (+)/inflammation (+) group] (Table 1). A representative case is shown in Figure 2A. The remaining 29 patients with atherosclerosis had no inflammation [atherosclerosis (+)/inflammation (–) group] (Table 1 and Figure 2B). Although inflammation was noted in a small subset of patients without atherosclerosis [atherosclerosis (–)/inflammation (+) group] (Table 1 and Figure 2C), the majority of patients without atherosclerosis did not have inflammation [atherosclerosis (–)/inflammation (–) group] (Table 1 and Figure 2D). The prevalence of inflammation was significantly higher in patients with atherosclerosis than in patients without (29 and 10%, respectively, P < 0.01, ² test).

View this table: [in this window] [in a new window]   Table 1 Patient profile

 

View larger version (46K): [in this window] [in a new window] [Download PowerPoint slide]   Figure 2 Representative 18F-fluorodeoxyglucose–positron emission tomography images and high-resolution B-mode carotid artery ultrasonography images of patients having carotid atherosclerosis with (A) and without FDG uptake or inflammation (B) and patients not having atherosclerosis with (C) and without inflammation (D). White arrow indicates vascular FDG uptake. Yellow arrow denotes carotid plaque. Notice that the ultrasonograms of plaques in (A) and (B) cannot tell whether they have inflammation or not.

 
Clinical characteristics
Clinical characteristics of each group are shown in Table 1. Body mass index, waist circumference, and the number of localized plaques were greater in inflammation (+) subset than that in inflammation (–) subset of atherosclerosis (+) patients. Other clinical variables did not differ among the four groups.

	Discussion

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 
The present study is the first prospective study with a large number of subjects, investigating the prevalence of inflammation in documented carotid atherosclerosis using the combination of CA-US and FDG–PET/CT imagings. We have demonstrated that inflammation is visualized by FDG–PET/CT imaging in 30% of the patients who have documented with carotid atherosclerosis but not having the history of recent CVD.

Methodological considerations
Although FDG uptake was detected in the area of the carotid artery, we performed contrast-enhanced CT and obtained PET/CT images in order to verify FDG uptake in the vessel wall. As shown in Figure 1, the strong FDG uptake was located in the vessel wall or atherosclerotic plaque. We did not have further information for the location of uptake because of spatial resolution. However, previous studies, which examined the endarterectomized specimen excised from the FDG uptake-documented carotid arteries, have provided histological validation that vascular FDG uptake is associated with the accumulation of inflammatory cells, especially macrophages, not only in symptomatic but also asymptomatic carotid plaques, irrespective of the severity of the luminal stenosis.^13–15 Moreover, our recent study has shown that carotid SUV level is significantly correlated with serum high-sensitivity C-reactive protein level in 216 subjects who underwent FDG–PET imaging for cancer screening.²² These findings suggest that the magnitude of FDG uptake would reflect the severity of carotid atherosclerotic inflammation.

Blood pool activity may be a possible source of FDG uptake. In our study, the possibility was unlikely because SUV of the jugular vein (blood uptake) was low and almost constant. Thus, we did not normalize SUV of the vascular wall by blood SUV for quantifying the FDG uptake. However, normalization by blood FDG uptake may give a more accurate estimation of the inflammation.¹⁵ Because of limited time available for PET imaging for a patient in our institution, PET imaging was performed 1 h after FDG injection. Longer time intervals would give clearer PET imaging.¹³

Prevalence of inflammation of carotid atherosclerosis
One-third of patients with atherosclerosis had inflammation of the carotid artery in this study (Table 1). However, the prevalence depends on the criteria of atherosclerosis by CA-US and of inflammation by FDG–PET. We performed CA-US and adopted the criterion of atherosclerosis by the presence of the plaque score 5 and/or the focal IMT 2 mm. A prospective follow-up study (OSACA study) showed that subjects with the plaque score 5 had the moderate to severe risk for the primary and recurrent ischaemic CVD with the annual incidences of 4.2 and 12% per year, respectively.²⁰ For vascular inflammation, we adopted the SUV score of 1.6, more than one times the SD above the average of the present study population. The score of 1.6 may have been reasonable because it was comparable with the SUV levels of several kinds of cancers.^23,24 Moreover, in patients with aortitis syndrome, the SUV 1.30 was shown to indicate active vessel inflammation with the sensitivity of 91% and the specificity of 89%.²⁵ However, the cut-off value for the identification of inflamed carotid artery may be reconsidered after collecting more data based on future studies with larger patient number. Our study is different from several previous ones^10–12 that reported the prevalence of FDG uptake to be 50–60% in the aorta and the iliac and femoral arteries in humans for the following points. First, the prevalence of FDG uptake in carotid artery has never been studied. Second, they performed FDG–PET or FDG–PET/CT imaging for patients for various clinical indications, mainly cancer diagnosis and staging, in whom the presence of atherosclerosis was unknown. We performed CA-US first, and thus the figure of 30% was for the prevalence of inflammation in documented carotid atherosclerosis. Third, we quantitatively estimated inflammation using SUV, whereas they only visually identified high FDG uptake.

High FDG uptake was detected in a small number of patients without significant atherosclerosis (Figure 2C). The mechanism and reason were not clear, but may have been explained by the early atherosclerotic changes such as fatty streaks. Another possible origin may be smooth muscle cells with increased metabolism in the media of arteriosclerotic vessels.¹⁰ In addition, the adventitia is a potential focus of the inflammation because adventitial accumulation of inflammatory cells plays a role in development of atherosclerosis.²⁶ This issue should be addressed in future clinical and experimental studies.

Risk factors of carotid inflammation in documented atherosclerosis
Discussion regarding risk factors of carotid inflammation is largely limited by the following reasons. First, the number of inflammation (+) patients was too small to analyse statistically. Second, this study included patients on aspirin, angiotensin receptor blocker or angiotensin converting enzyme inhibitor therapy, which may attenuate inflammation, because it is not ethically feasible to discontinue these medications.

As shown in Table 1, the inflammation (+) subset had greater body mass index, waist circumference, and the prevalence of antihypertensive medications than the inflammation (–) subset of atherosclerosis (+) patients. These observations were consistent with our recent study showing that carotid FDG uptake was associated with the components of the metabolic syndrome in patients who underwent FDG–PET imaging for cancer screening.²² It was noteworthy that waist circumference was the strongest determinant factor of the FDG uptake and the second one was antihypertensive medication in our recent study.²² However, a future study with a large number of patients is warranted to clarify the factors of inflammation of documented carotid atherosclerosis.

Limitation of this study
Currently, there is no gold standard available for the identification of inflammation of local vascular lesions. Histological verification of inflammation would strengthen our present findings. In this study, however, it was ethically not feasible to obtain histological samples in the corresponding carotid plaques because of the lack of clinical indication for endoarterectomy. Thus, it is impossible to provide the data regarding the sensitivity and specificity of FDG–PET imaging in detecting inflammation of carotid atherosclerosis at present. Another limitation of this study was the lack of the associations between the FDG uptake levels and the morphological features, such as size, ulceration, irregularity, and echogenicity, plaque by plaque. Most individual lesions detected by US-CA cannot readily be identified by PET/CT imaging because of the limited spatial resolution. Thus, we measured the SUV score of the carotid arteries but not of individual plaques. Finally, the use of PET combined with high-resolution MRI or a hybrid PET/CT would improve the accuracy of localization of FDG uptake.

Perspectives
The present study has for the first time demonstrated that 30% of patients with documented carotid atherosclerosis have inflammation detected by FDG–PET imaging. This raises the possibility that this non-invasive, metabolic imaging modality would aid in the risk stratification and the selection of appropriate therapy, such as intensive medical therapy, carotid stenting, and carotid endarterectomy, of patients at risk of strokes. For this purpose, a prospective study is necessary to determine if the detection of inflamed plaque by FDG–PET imaging is useful for predicting future CVD.

	Acknowledgements

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 
This study was supported in part by a research grant from the Kimura Memorial Foundation (T.I.); by grants from the Ishibashi Foundation for the Promotion of Science (N.T.), Fukuda Foundation for Medical Technology (N.T.), Mitsui Life Social Welfare Foundation (N.T.), and Japan Heart Foundation Research (N.T.); and by a grant for the Academic Frontier Project from the Ministry of Education, Science, Sports, Culture, and Technology, Japan (Cardiovascular Research Institute, Kurume University).

Conflict of interest: none declared.

	References

Top Abstract Introduction Methods Results Discussion Acknowledgements References

 

1. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med (1999) 340:115–126.[Free Full Text]
2. Fleming RM. The pathogenesis of vascular disease. In: Textbook of Angiology—Chang JC, ed. (1999) New York: Springer-Verlag. 787–798.
3. Libby P. Inflammation in atherosclerosis. Nature (2002) 420:868–874.[CrossRef][Medline]
4. Lusis AJ. Atherosclerosis. Nature (2000) 407:233–241.[CrossRef][Medline]
5. Ridker PM, Rifai N, Clearfield M, Downs JR, Weis SE, Miles JS, Gotto AM Jr, Air Force/Texas Coronary Atherosclerosis Prevention Study Investigators. Measurement of C-reactive protein for the targeting of statin therapy in the primary prevention of acute coronary events. N Engl J Med (2001) 344:1959–1965.[Abstract/Free Full Text]
6. Ridker PM, Rifai N, Pfeffer MA, Sacks F, Braunwald E. Long-term effects of pravastatin on plasma concentration of C-reactive protein. The cholesterol and recurrent events (care) investigators. Circulation (1999) 100:230–235.[Abstract/Free Full Text]
7. Salonen JT, Salonen R. Ultrasound B-mode imaging in observational studies of atherosclerotic progression. Circulation (1993) 87(Suppl. II):II-56–II-65.[Medline]
8. Nighoghossian N, Derex L, Douek P. The vulnerable carotid artery plaque: current imaging methods and new perspectives. Stroke (2005) 36:2764–1772.[Abstract/Free Full Text]
9. Blockmans D, Maes A, Stroobants S, Nuyts J, Bormans G, Knockaert D, Bobbaers H, Mortelmans L. New arguments for a vasculitic nature of polymyalgia rheumatica using positron emission tomography. Rheumatology (Oxford) (1999) 38:444–447.[CrossRef][Medline]
10. Yun M, Jang S, Cucchiara A, Newberg AB, Alavi A. 18F FDG uptake in the large arteries: a correlation study with the atherogenic risk factors. Semin Nucl Med (2002) 32:70–76.[CrossRef][Web of Science][Medline]
11. Yun M, Yeh D, Araujo LI, Jang S, Newberg A, Alavi A. F-18 FDG uptake in the large arteries: a new observation. Clin Nucl Med (2001) 26:314–319.[CrossRef][Web of Science][Medline]
12. Tatsumi M, Cohade C, Nakamoto Y, Wahl RL. Fluorodeoxyglucose uptake in the aortic wall at PET/CT: possible finding for active atherosclerosis. Radiology (2003) 229:831–837.[Abstract/Free Full Text]
13. Rudd JH, Warburton EA, Fryer TD, Jones HA, Clark JC, Antoun N, Johnstrom P, Davenport AP, Kirkpatrick PJ, Arch BN, Pickard JD, Weissberg PL. Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation (2002) 105:2708–2711.[Abstract/Free Full Text]
14. Davies JR, Rudd JH, Fryer TD, Graves MJ, Clark JC, Kirkpatrick PJ, Gillard JH, Warburton EA, Weissberg PL. Identification of culprit lesions after transient ischemic attack by combined 18F fluorodeoxyglucose positron-emission tomography and high-resolution magnetic resonance imaging. Stroke (2005) 36:2642–2647.[Abstract/Free Full Text]
15. Tawakol A, Migrino RQ, Bashian GG, Bedri S, Vermylen D, Cury RC, Yates D, LaMuraglia GM, Furie K, Houser S, Gewirtz H, Muller JE, Brady TJ, Fischman AJ. In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol (2006) 48:1818–1824.[Abstract/Free Full Text]
16. Egashira K. Molecular mechanisms mediating inflammation in vascular disease: special reference to monocyte chemoattractant protein-1. Hypertension (2003) 41:834–841.[Abstract/Free Full Text]
17. Tahara N, Kai H, Ishibashi M, Nakaura H, Kaida H, Baba K, Hayabuchi N, Imaizumi T. Simvastatin attenuates plaque inflammation—evaluation by fluorodeoxyglucose positron emission tomography. J Am Coll Cardiol (2006) 48:1825–1831.[Abstract/Free Full Text]
18. Cockcroft DW, Gault MH. Prediction of creatinine clearance from serum creatinine. Nephron (1976) 16:31–41.[Web of Science][Medline]
19. Handa N, Matsumoto M, Maeda H, Hougaku H, Ogawa S, Fukunaga R, Yoneda S, Kimura K, Kamada T. Ultrasonic evaluation of early carotid atherosclerosis. Stroke (1990) 21:1567–1572.[Abstract/Free Full Text]
20. Handa N, Matsumoto M, Maeda H, Hougaku H, Kamada T. Ischemic stroke events and carotid atherosclerosis. Results of the Osaka follow-up study for ultrasonographic assessment of carotid atherosclerosis (the OSACA study). Stroke (1995) 26:1781–1786.[Abstract/Free Full Text]
21. Pignoli P, Tremoli E, Poli A, Oreste P, Paoletti R. Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation (1986) 74:1399–1406.[Abstract/Free Full Text]
22. Tahara N, Kai H, Yamagishi S, Mizoguchi M, Nakaura H, Ishibashi M, Kaida H, Baba K, Hayabuchi N, Imaizumi T. Vascular inflammation evaluated by [18F]-fluorodeoxyglucose positron emission tomography is associated with the metabolic syndrome. J Am Coll Cardiol (2007) 49:1533–1539.[Abstract/Free Full Text]
23. Chen J, Cheong JH, Yun MJ, Kim J, Lim JS, Hyung WJ, Noh SH. Improvement in preoperative staging of gastric adenocarcinoma with positron emission tomography. Cancer (2005) 103:2383–2390.[CrossRef][Web of Science][Medline]
24. Kim TY, Kim WB, Ryu JS, Gong G, Hong SJ, Shong YK. 18F-fluorodeoxyglucose uptake in thyroid from positron emission tomogram (PET) for evaluation in cancer patients: high prevalence of malignancy in thyroid PET incidentaloma. Laryngoscope (2005) 115:1074–1078.[CrossRef][Web of Science][Medline]
25. Kobayashi Y, Ishii K, Oda K, Nariai T, Tanaka Y, Ishiwata K, Numano F. Aortic wall inflammation due to takayasu arteritis imaged with 18F-FDG PET coregistered with enhanced CT. J Nucl Med (2005) 46:917–922.[Abstract/Free Full Text]
26. Wilcox JN, Scott NA. Potential role of the adventitia in arteritis and atherosclerosis. Int J Cardiol (1996) 54:S21–S35.[CrossRef][Web of Science][Medline]

CiteULike    Connotea    Del.icio.us    What's this?

This article has been cited by other articles:

				J. H.F. Rudd, F. Hyafil, and Z. A. Fayad Inflammation Imaging in Atherosclerosis Arterioscler. Thromb. Vasc. Biol., July 1, 2009; 29(7): 1009 - 1016. [Abstract] [Full Text] [PDF]

				L. J. Menezes, C. W. Kotze, B. F. Hutton, R. Endozo, J. C. Dickson, I. Cullum, S. W. Yusuf, P. J. Ell, and A. M. Groves Vascular Inflammation Imaging with 18F-FDG PET/CT: When to Image? J. Nucl. Med., June 1, 2009; 50(6): 854 - 857. [Abstract] [Full Text] [PDF]

				N. Tahara, T. Imaizumi, R. Virmani, and J. Narula Clinical Feasibility of Molecular Imaging of Plaque Inflammation in Atherosclerosis J. Nucl. Med., March 1, 2009; 50(3): 331 - 334. [Abstract] [Full Text] [PDF]

				J. H.F. Rudd, K. S. Myers, S. Bansilal, J. Machac, M. Woodward, V. Fuster, M. E. Farkouh, and Z. A. Fayad Relationships Among Regional Arterial Inflammation, Calcification, Risk Factors, and Biomarkers: A Prospective Fluorodeoxyglucose Positron-Emission Tomography/Computed Tomography Imaging Study Circ Cardiovasc Imaging, March 1, 2009; 2(2): 107 - 115. [Abstract] [Full Text] [PDF]

				E. Falk, T. Thim, and I. B. Kristensen Atherosclerotic plaque, adventitia, perivascular fat, and carotid imaging. J. Am. Coll. Cardiol. Img., February 1, 2009; 2(2): 183 - 186. [Full Text] [PDF]

				E. A. Osborn and F. A. Jaffer The year in molecular imaging. J. Am. Coll. Cardiol. Img., January 1, 2009; 2(1): 97 - 113. [Full Text] [PDF]

This Article Abstract FREE Full Text (PDF) All Versions of this Article: 28/18/2243    most recent ehm245v1 E-letters: Submit a response Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (1) Request Permissions Disclaimer Google Scholar Articles by Tahara, N. Articles by Imaizumi, T. Search for Related Content PubMed PubMed Citation Articles by Tahara, N. Articles by Imaizumi, T. Social Bookmarking          What's this?

Online ISSN 1522-9645 - Print ISSN 0195-668x

Copyright © 2009 European Society of Cardiology

Oxford Journals Oxford University Press

• Site Map
• Privacy Policy
• Frequently Asked Questions

Other Oxford University Press sites: Oxford University Press Oxford Journals China Oxford Journals Japan American National Biography Booksellers' Information Service Children's Fiction and Poetry Children's Reference Corporate & Special Sales Dictionaries Dictionary of National Biography Digital Reference English Language Teaching Higher Education Textbooks Humanities International Education Unit Law Medicine Music Online Products Oxford English Dictionary Reference Rights and Permissions Science School Books Social Sciences Very Short Introductions World's Classics