18 F-Fluorodeoxyglucose Imaging of Inflammation
2017; Lippincott Williams & Wilkins; Volume: 10; Issue: 3 Linguagem: Inglês
10.1161/circimaging.117.006185
ISSN1942-0080
AutoresGianmario Sambuceti, Silvia Morbelli, Anna Maria Orengo, Matteo Bauckneht, Cecilia Marini,
Tópico(s)Streptococcal Infections and Treatments
ResumoHomeCirculation: Cardiovascular ImagingVol. 10, No. 318F-Fluorodeoxyglucose Imaging of Inflammation Free AccessEditorialPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessEditorialPDF/EPUB18F-Fluorodeoxyglucose Imaging of InflammationReady to Represent a Standard in Diagnosing Endocarditis? Gianmario Sambuceti, MD, Silvia Morbelli, MD, PhD, Anna Maria Orengo, BS, Matteo Bauckneht, MD and Cecilia Marini, MD, PhD Gianmario SambucetiGianmario Sambuceti From the Department of Health Sciences, University of Genoa, Italy (G.S., M.B.); Nuclear Medicine Unit, IRCCS San Martino-IST, Genoa, Italy (G.S., S.M., A.M.O., C.M.); and CNR Institute of Bioimages and Molecular Physiology, Milan, Italy (C.M.). , Silvia MorbelliSilvia Morbelli From the Department of Health Sciences, University of Genoa, Italy (G.S., M.B.); Nuclear Medicine Unit, IRCCS San Martino-IST, Genoa, Italy (G.S., S.M., A.M.O., C.M.); and CNR Institute of Bioimages and Molecular Physiology, Milan, Italy (C.M.). , Anna Maria OrengoAnna Maria Orengo From the Department of Health Sciences, University of Genoa, Italy (G.S., M.B.); Nuclear Medicine Unit, IRCCS San Martino-IST, Genoa, Italy (G.S., S.M., A.M.O., C.M.); and CNR Institute of Bioimages and Molecular Physiology, Milan, Italy (C.M.). , Matteo BaucknehtMatteo Bauckneht From the Department of Health Sciences, University of Genoa, Italy (G.S., M.B.); Nuclear Medicine Unit, IRCCS San Martino-IST, Genoa, Italy (G.S., S.M., A.M.O., C.M.); and CNR Institute of Bioimages and Molecular Physiology, Milan, Italy (C.M.). and Cecilia MariniCecilia Marini From the Department of Health Sciences, University of Genoa, Italy (G.S., M.B.); Nuclear Medicine Unit, IRCCS San Martino-IST, Genoa, Italy (G.S., S.M., A.M.O., C.M.); and CNR Institute of Bioimages and Molecular Physiology, Milan, Italy (C.M.). Originally published15 Mar 2017https://doi.org/10.1161/CIRCIMAGING.117.006185Circulation: Cardiovascular Imaging. 2017;10For >100 years,1 the diagnosis of endocarditis has been challenging, and this has been compounded by the increasing number of patients with prosthetic materials in the heart. The clinical challenge extends beyond accuracy because any delay in disease recognition inevitably postpones treatment planning and contributes to the high mortality rate that ranges between 14% and 22% during the hospitalization and ≤40% at 1-year follow-up.2 Current standards rely on the modified Duke criteria3 that catalogues clinical, imaging, microbiological, and pathological data into major and minor criteria so as to define a diagnostic probability classified as definite, possible, or unlikely with a sensitivity of ≈80%.4 Echocardiography (either transthoracic or transesophageal) represents an essential component in this process. However, despite its high resolution and wide applicability, ultrasound imaging is limited, particularly under 2 different conditions: in early disease stages, small structural alterations can be missed, whereas in postsurgical patients, the presence of composite material generates acoustic shadowing that may hamper diagnosis of prosthetic valve endocarditis (PVE),5 leading to inconclusive diagnosis in about 30% of patients.6See Article by Mathieu et alTo overcome this clinical uncertainty, single photon emission computed tomographic imaging of labeled leukocyte recruitment has been used for quite some time as a means to detect focal areas of infection.7,8 Overall consensus is that this technique is highly specific both in endocarditis of native structures and in PVE. However, the limited spatial resolution limits its diagnostic sensitivity even when single photon emission computed tomography is coregistered with computed tomography (CT). Radiolabeling of white blood cells also adds complexity to this procedure. Consequently, it tends to be used when other approaches remain inconclusive unless the question of endocarditis occurs in the early postsurgical phases, when the healing process impedes the analysis of other signals of infection.9More recently, PET/CT imaging and its capability to document the high avidity of inflammatory infiltrates for 18F-fluorodeoxyglucose (FDG) has emerged as an alternative diagnostic tool.6,10–13 The clinical potential of this approach has been tested in a relatively large number of studies and has been officially accepted by the European Society of Cardiology whose guidelines, published in August 2015,14 propose an abnormal uptake of FDG in the location of the implant as a new major diagnostic criterion for PVE if documented >3 months after surgery. However, this decision has not been shared by the American Heart Association that explicitly requested a larger clinical experience to better define the potential role of FDG PET/CT imaging in the management of these patients.15In this issue of Circulation: Cardiovascular Imaging, Mathieu et al16 approached this discrepancy in a unique manner. The authors evaluated a series of 51 patients with prosthetic heart valves (PHV), referred to FDG PET/CT imaging for clinical reasons unrelated to a possible infection or with suspected and subsequently excluded PVE. The study aimed to characterize frequency and pattern of visible FDG uptake after uncomplicated valvular replacement as to reduce the incidence of false-positive diagnoses. However, this same analysis provides data whose relevance probably extends beyond this specific purpose and raises issues about patient preparation, image reconstruction, and interpretation.Patient PreparationIn routine oncological application of FDG PET/CT, many patients display visible myocardial uptake even under fasting condition. The heterogeneous distribution of FDG uptake, associated with the blurring effect caused by cardiac and respiratory motion,17 can either mask or (though less frequently) simulate a local infection. To minimize this confounding effect, several authors proposed a prolonged reduction in sugar intake.9,10 This dietary regimen does not modify metabolism of inflammatory infiltrates because transmembrane sugar transport in white blood cells relies on the constitutive availability of GLUT1 and GLUT3. By contrast, the prolonged decrease in serum glucose and insulin levels lowers myocardial glucose consumption, by lowering GLUT4 docking to the sarcolemma. If maintained for an adequate time span, this metabolic pattern is further amplified by the increase in intracellular concentration of free fatty acid derivatives. According to the Randle cycle,18 this condition activates the peroxisome proliferator-activated receptor-α that transcriptionally promotes the expression of enzymes governing fatty acid metabolism further reducing glycolytic flux and thus FDG uptake by normal myocytes.19The relevance of this pathway in allowing an adequate infection:background ratio has been recently reported by Scholtens et al20: preceding tracer injection by 12 hours of carbohydrate-restricted, fat-allowed, and protein-allowed diet followed by 12 hours fasting period resulted in an absent cardiac uptake in 54% of patients compared with 28% of subjects studied with the standard 6 hours fasting protocol. Adding a single bolus of heparin (50 IU/kg)—whose lipolytic activity can induce a 5-fold increase in blood free fatty acid levels21—before FDG administration further increased this response ≤88%. Intriguingly, the performance of a complex dietary preparation is not far from the one reported by Mathieu et al16 in a much larger population. Because of the retrospective nature, the study evaluated patients submitted to the conventional protocol with only 6 hours fasting before tracer injection. Nevertheless, cardiac FDG uptake was as low as to allow the evaluation of prosthetic material in 495 of 585 patients (85%).The comparison between these 2 reports indicates that despite its robust theoretical basis, current protocols aiming to optimize patient preparation might have a relatively limited impact on diagnostic accuracy of FDG imaging. Accordingly, it points out the need for further studies to verify the clinical performance of currently proposed protocols implying 12 hours fasting preceded by a sugar free diet for 12 hours without any further intervention9,10 or for 48 hours and combined with heparin administration.22Timing After SurgeryOne of most acknowledged clinical conditions that impacts the accuracy of FDG imaging in PVE is the time from surgery. Actually, PHV implantation activates a series of host tissue reactions characterized by an enhanced migratory and proliferative potential of inflammatory cells, myofibroblasts, and capillary endothelial cells.23 This sequence of events increases FDG uptake in the perivalvular area even in the absence of infection early after valve surgery. This metabolic activation slows down in later phases when the progression of the healing process leads to the formation of a fibrous cuff with increasing amounts of collagen and re-endothelialization of the sewing ring. On the basis of these theoretical considerations, the European Society of Cardiology guidelines suggest a diagnostic role for FDG positron emission tomography (PET)/CT imaging only >3 months after surgery. However, the duration of this process can be variable and can extend ≤1 year in prosthetic valves24 in the absence of a clinically recognizable infection.In agreement with this concept, in this study by Mathieu et al,16 periprosthetic FDG uptake was almost independent from the time elapsed between surgery and the FDG PET scan in patients free from PVE. Similarly, in a study by Jiménez-Ballvé,22 incidence of false-positive FDG uptake even decreased from 15% to 9% in patients studied >1 year or 3 months).Attenuation CorrectionMetallic components can cause artifacts because of overcorrection of photon attenuation17,18,22 that limits the evaluation of both mechanical and, though to a lesser degree, biological PHV. To overcome this limitation, several authors proposed to consider the persistence of visible uptake in both attenuation corrected (AC) and non-AC (NAC) images as an essential criterion for PVE.9,11,25–27 Jiménez-Ballvé22 addressed this issue in 41 patients with suspected PVE. The gold standard for diagnosis was the Duke pathological criteria or the decision of an endocarditis expert team after a minimum 4 months follow-up. Evaluation of AC images showed a really poor diagnostic accuracy (sensitivity 100%, specificity 20%). However, diagnostic potential was significantly improved when increased FDG uptake persisted on NAC data. In fact, the combined analysis of both image sets showed an excellent sensitivity (100%) with an intermediate specificity (73%).The study by Mathieu et al16 strongly confirms this assumption. In fact, PHV FDG uptake was visible in 87% of AC images despite the absence of any clinically relevant infection. This prevalence significantly decreased to 56% when NAC images were analyzed. Accordingly, combined analysis of AC and NAC images seems a mandatory step to reduce the number of false-positive studies.FDG Uptake PatternOne of the most relevant advantages of FDG PET/CT imaging is its capability to accurately quantify tracer concentration by the so-called standardized uptake value. However, the specific setting of PVE amplifies the ongoing debate that characterizes the use of this index in oncology because of its multifactorial nature. Actually, Sarrazin et al26 reported that maximal standardized uptake value was 4.4±1.6 in patients with high suspicion of PVE as opposed to 1.2±1.4 in negative studies, suggesting that quantitative indexes of FDG uptake might definitely contribute to PVE diagnosis. However, this statement has not been confirmed by other authors.22In the study of Mathieu et al,16 estimated standardized uptake value max of noninfected PHVs ranged from 3 to 8 and 2.1 to 5.7 in patients with or without concomitant vasculitis, respectively, corroborating the concept that standardized uptake value max is probably an inaccurate criterion for PVE diagnosis. Importantly, this study found that the pattern of FDG uptake was more useful for excluding infection in noninfected PHVs, thereby reducing the incidence of false-positive results. Indeed, FDG uptake was relatively homogeneous in these patients free from clinically relevant infection. By contrast, focal hot spots that are more suggestive of infection were relatively rare occurring in only 7% and 6% of AC and NAC images, respectively. Despite this impressive result, the robustness of this criterion still needs more formal evaluation because both cardiac and respiratory motion can potentially lead to artifacts that affect the appearance of FDG retention. In this regard, the potential of gated acquisition might represent a relevant step forward in this process.28In conclusion, PET/CT imaging has great potential in PVE diagnosis even without considering the opportunity to visualize the whole body for detection of septic embolization. However, further studies are needed to identify optimal protocols for patient preparation and for image acquisition, reconstruction, and interpretation. This preliminary work seems mandatory for the correct placement of FDG imaging in the clinical management of these patients.DisclosuresNone.FootnotesThe opinions expressed in this article are not necessarily those of the editors or of the American Heart Association.Correspondence to Gianmario Sambuceti, MD, Nuclear Medicine, IRCCS San Martino, IST Department of Health Science, University of Genoa Viale Pastore 1, 16132 Genova, Italy. E-mail [email protected]References1. Osler W. The Gulstonian Lectures, on malignant endocarditis.Br Med J. 1885; 1:577–579.CrossrefMedlineGoogle Scholar2. Thuny F, Giorgi R, Habachi R, Ansaldi S, Le Dolley Y, Casalta JP, Avierinos JF, Riberi A, Renard S, Collart F, Raoult D, Habib G. Excess mortality and morbidity in patients surviving infective endocarditis.Am Heart J. 2012; 164:94–101. doi: 10.1016/j.ahj.2012.04.003.CrossrefMedlineGoogle Scholar3. Li JS, Sexton DJ, Mick N, Nettles R, Fowler VG, Ryan T, Bashore T, Corey GR. 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