Publications by authors named "Riemer H J A Slart"

279 Publications

EARL compliance and imaging optimisation on the Biograph Vision Quadra PET/CT using phantom and clinical data.

Eur J Nucl Med Mol Imaging 2022 Jul 25. Epub 2022 Jul 25.

Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Purpose: Current European Association of Nuclear Medicine (EANM) Research Ltd. (EARL) guidelines for the standardisation of PET imaging developed for conventional systems have not yet been adjusted for long axial field-of-view (LAFOV) systems. In order to use the LAFOV Siemens Biograph Vision Quadra PET/CT (Siemens Healthineers, Knoxville, TN, USA) in multicentre research and harmonised clinical use, compliance to EARL specifications for F-FDG tumour imaging was explored in the current study. Additional tests at various locations throughout the LAFOV and the use of shorter scan durations were included. Furthermore, clinical data were collected to further explore and validate the effects of reducing scan duration on semi-quantitative PET image biomarker accuracy and precision when using EARL-compliant reconstruction settings.

Methods: EARL compliance phantom measurements were performed using the NEMA image quality phantom both in the centre and at various locations throughout the LAFOV. PET data (maximum ring difference (MRD) = 85) were reconstructed using various reconstruction parameters and reprocessed to obtain images at shorter scan durations. Maximum, mean and peak activity concentration recovery coefficients (RC) were obtained for each sphere and compared to EARL standards specifications. Additionally, PET data (MRD = 85) of 10 oncological patients were acquired and reconstructed using various reconstruction settings and reprocessed from 10 min listmode acquisition into shorter scan durations. Per dataset, SUVs were derived from tumour lesions and healthy tissues. ANOVA repeated measures were performed to explore differences in lesion SUV and SUV. Wilcoxon signed-rank tests were performed to evaluate differences in background SUV and SUV between scan durations. The coefficient of variation (COV) was calculated to characterise noise.

Results: Phantom measurements showed EARL compliance for all positions throughout the LAFOV for all scan durations. Regarding patient data, EARL-compliant images showed no clinically meaningful significant differences in lesion SUV and SUV or background SUV and SUV between scan durations. Here, COV only varied slightly.

Conclusion: Images obtained using the Vision Quadra PET/CT comply with EARL specifications. Scan duration and/or activity administration can be reduced up to a factor tenfold without the interference of increased noise.
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http://dx.doi.org/10.1007/s00259-022-05919-1DOI Listing
July 2022

Hot spot imaging in cardiovascular diseases: an information statement from SNMMI, ASNC, and EANM.

J Nucl Cardiol 2022 Jul 21. Epub 2022 Jul 21.

Department of Radiology and Biomedical Imaging, Yale University, 801 Howard Ave, New Haven, CT, 06519, USA.

This information statement from the Society of Nuclear Medicine and Molecular Imaging, American Society of Nuclear Cardiology, and European Association of Nuclear Medicine describes the performance, interpretation, and reporting of hot spot imaging in nuclear cardiology. The field of nuclear cardiology has historically focused on cold spot imaging for the interpretation of myocardial ischemia and infarction. Hot spot imaging has been an important part of nuclear medicine, particularly for oncology or infection indications, and the use of hot spot imaging in nuclear cardiology continues to expand. This document focuses on image acquisition and processing, methods of quantification, indications, protocols, and reporting of hot spot imaging. Indications discussed include myocardial viability, myocardial inflammation, device or valve infection, large vessel vasculitis, valve calcification and vulnerable plaques, and cardiac amyloidosis. This document contextualizes the foundations of image quantification and highlights reporting in each indication for the cardiac nuclear imager.
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http://dx.doi.org/10.1007/s12350-022-02985-8DOI Listing
July 2022

Detecting the vulnerable carotid plaque: the Carotid Artery Multimodality imaging Prognostic study design.

J Cardiovasc Med (Hagerstown) 2022 07 23;23(7):466-473. Epub 2022 Jun 23.

Cardiology Unit, Cardio-Thoracic and Vascular Department, University of Pisa, Pisa, Italy.

Background: Carotid artery disease is highly prevalent and a main cause of ischemic stroke and vascular dementia. There is a paucity of information on predictors of serious vascular events. Besides percentage diameter stenosis, international guidelines also recommend the evaluation of qualitative characteristics of carotid artery disease as a guide to treatment, but with no agreement on which qualitative features to assess. This inadequate knowledge leads to a poor ability to identify patients at risk, dispersion of medical resources, and unproven use of expensive and resource-consuming techniques, such as magnetic resonance imaging, positron emission tomography, and computed tomography.

Objectives: The Carotid Artery Multimodality imaging Prognostic (CAMP) study will: prospectively determine the best predictors of silent and overt ischemic stroke and vascular dementia in patients with asymptomatic subcritical carotid artery disease by identifying the noninvasive diagnostic features of the 'vulnerable carotid plaque'; assess whether 'smart' use of low-cost diagnostic methods such as ultrasound-based evaluations may yield at least the same level of prospective information as more expensive techniques.

Study Design: We will compare the prognostic/predictive value of all proposed techniques with regard to silent or clinically manifest ischemic stroke and vascular dementia. The study will include ≥300 patients with asymptomatic, unilateral, intermediate degree (40-60% diameter) common or internal carotid artery stenosis detected at carotid ultrasound, with a 2-year follow-up. The study design has been registered on Clinicaltrial.gov on December 17, 2020 (ID number NCT04679727).
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http://dx.doi.org/10.2459/JCM.0000000000001314DOI Listing
July 2022

Use of [C]choline PET/CT for visualization of four hyperactive parathyroid glands in a patient with renal hyperparathyroidism.

Eur J Nucl Med Mol Imaging 2022 Jun 28. Epub 2022 Jun 28.

Medical Imaging Center, Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Hanzeplein 1, 9700, RB, Groningen, The Netherlands.

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http://dx.doi.org/10.1007/s00259-022-05885-8DOI Listing
June 2022

Novel PET Imaging of Inflammatory Targets and Cells for the Diagnosis and Monitoring of Giant Cell Arteritis and Polymyalgia Rheumatica.

Front Med (Lausanne) 2022 6;9:902155. Epub 2022 Jun 6.

Department of Rheumatology and Clinical Immunology, University of Groningen, University Medical Center Groningen, Groningen, Netherlands.

Giant cell arteritis (GCA) and polymyalgia rheumatica (PMR) are two interrelated inflammatory diseases affecting patients above 50 years of age. Patients with GCA suffer from granulomatous inflammation of medium- to large-sized arteries. This inflammation can lead to severe ischemic complications (e.g., irreversible vision loss and stroke) and aneurysm-related complications (such as aortic dissection). On the other hand, patients suffering from PMR present with proximal stiffness and pain due to inflammation of the shoulder and pelvic girdles. PMR is observed in 40-60% of patients with GCA, while up to 21% of patients suffering from PMR are also affected by GCA. Due to the risk of ischemic complications, GCA has to be promptly treated upon clinical suspicion. The treatment of both GCA and PMR still heavily relies on glucocorticoids (GCs), although novel targeted therapies are emerging. Imaging has a central position in the diagnosis of GCA and PMR. While [F]fluorodeoxyglucose (FDG)-positron emission tomography (PET) has proven to be a valuable tool for diagnosis of GCA and PMR, it possesses major drawbacks such as unspecific uptake in cells with high glucose metabolism, high background activity in several non-target organs and a decrease of diagnostic accuracy already after a short course of GC treatment. In recent years, our understanding of the immunopathogenesis of GCA and, to some extent, PMR has advanced. In this review, we summarize the current knowledge on the cellular heterogeneity in the immunopathology of GCA/PMR and discuss how recent advances in specific tissue infiltrating leukocyte and stromal cell profiles may be exploited as a source of novel targets for imaging. Finally, we discuss prospective novel PET radiotracers that may be useful for the diagnosis and treatment monitoring in GCA and PMR.
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http://dx.doi.org/10.3389/fmed.2022.902155DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9207253PMC
June 2022

Performance of visual, manual, and automatic coronary calcium scoring of cardiac N-ammonia PET/low dose CT.

J Nucl Cardiol 2022 Jun 16. Epub 2022 Jun 16.

Department of Nuclear Medicine, Northwest Clinics, Alkmaar, The Netherlands.

Background: Coronary artery calcium is a well-known predictor of major adverse cardiac events and is usually scored manually from dedicated, ECG-triggered calcium scoring CT (CSCT) scans. In clinical practice, a myocardial perfusion PET scan is accompanied by a non-ECG triggered low dose CT (LDCT) scan. In this study, we investigated the accuracy of patients' cardiovascular risk categorisation based on manual, visual, and automatic AI calcium scoring using the LDCT scan.

Methods: We retrospectively enrolled 213 patients. Each patient received a N-ammonia PET scan, an LDCT scan, and a CSCT scan as the gold standard. All LDCT and CSCT scans were scored manually, visually, and automatically. For the manual scoring, we used vendor recommended software (Syngo.via, Siemens). For visual scoring a 6-points risk scale was used (0; 1-10; 11-100; 101-400; 401-100; > 1 000 Agatston score). The automatic scoring was performed with deep learning software (Syngo.via, Siemens). All manual and automatic Agatston scores were converted to the 6-point risk scale. Manual CSCT scoring was used as a reference.

Results: The agreement of manual and automatic LDCT scoring with the reference was low [weighted kappa 0.59 (95% CI 0.53-0.65); 0.50 (95% CI 0.44-0.56), respectively], but the agreement of visual LDCT scoring was strong [0.82 (95% CI 0.77-0.86)].

Conclusions: Compared with the gold standard manual CSCT scoring, visual LDCT scoring outperformed manual LDCT and automatic LDCT scoring.
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http://dx.doi.org/10.1007/s12350-022-03018-0DOI Listing
June 2022

DeepStrain Evidence of Asymptomatic Left Ventricular Diastolic and Systolic Dysfunction in Young Adults With Cardiac Risk Factors.

Front Cardiovasc Med 2022 11;9:831080. Epub 2022 Apr 11.

Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, United States.

Purpose: To evaluate if a fully-automatic deep learning method for myocardial strain analysis based on magnetic resonance imaging (MRI) cine images can detect asymptomatic dysfunction in young adults with cardiac risk factors.

Methods: An automated workflow termed DeepStrain was implemented using two U-Net models for segmentation and motion tracking. DeepStrain was trained and tested using short-axis cine-MRI images from healthy subjects and patients with cardiac disease. Subsequently, subjects aged 18-45 years were prospectively recruited and classified among age- and gender-matched groups: risk factor group (RFG) 1 including overweight without hypertension or type 2 diabetes; RFG2 including hypertension without type 2 diabetes, regardless of overweight; RFG3 including type 2 diabetes, regardless of overweight or hypertension. Subjects underwent cardiac short-axis cine-MRI image acquisition. Differences in DeepStrain-based left ventricular global circumferential and radial strain and strain rate among groups were evaluated.

Results: The cohort consisted of 119 participants: 30 controls, 39 in RFG1, 30 in RFG2, and 20 in RFG3. Despite comparable (>0.05) left-ventricular mass, volumes, and ejection fraction, all groups (RFG1, RFG2, RFG3) showed signs of asymptomatic left ventricular diastolic and systolic dysfunction, evidenced by lower circumferential early-diastolic strain rate (<0.05, <0.001, <0.01), and lower septal circumferential end-systolic strain (<0.001, <0.05, <0.001) compared with controls. Multivariate linear regression showed that body surface area correlated negatively with all strain measures (<0.01), and mean arterial pressure correlated negatively with early-diastolic strain rate (<0.01).

Conclusion: DeepStrain fully-automatically provided evidence of asymptomatic left ventricular diastolic and systolic dysfunction in asymptomatic young adults with overweight, hypertension, and type 2 diabetes risk factors.
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http://dx.doi.org/10.3389/fcvm.2022.831080DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9035693PMC
April 2022

Development of a dynamic myocardial perfusion phantom model for tracer kinetic measurements.

EJNMMI Phys 2022 Apr 25;9(1):31. Epub 2022 Apr 25.

Robotics and Mechatronics (RaM) Group, Faculty of Electrical Engineering Mathematics and Computer Science, University of Twente, Enschede, The Netherlands.

Background: Absolute myocardial perfusion imaging (MPI) is beneficial in the diagnosis and prognosis of patients with suspected or known coronary artery disease. However, validation and standardization of perfusion estimates across centers is needed to ensure safe and adequate integration into the clinical workflow. Physical myocardial perfusion models can contribute to this clinical need as these can provide ground-truth validation of perfusion estimates in a simplified, though controlled setup. This work presents the design and realization of such a myocardial perfusion phantom and highlights initial performance testing of the overall phantom setup using dynamic single photon emission computed tomography.

Results: Due to anatomical and (patho-)physiological representation in the 3D printed myocardial perfusion phantom, we were able to acquire 22 dynamic MPI datasets in which Tc-labelled tracer kinetics was measured and analyzed using clinical MPI software. After phantom setup optimization, time activity curve analysis was executed for measurements with normal myocardial perfusion settings (1.5 mL/g/min) and with settings containing a regional or global perfusion deficit (0.8 mL/g/min). In these measurements, a specific amount of activated carbon was used to adsorb radiotracer in the simulated myocardial tissue. Such mimicking of myocardial tracer uptake and retention over time satisfactorily matched patient tracer kinetics. For normal perfusion levels, the absolute mean error between computed myocardial blood flow and ground-truth flow settings ranged between 0.1 and 0.4 mL/g/min.

Conclusion: The presented myocardial perfusion phantom is a first step toward ground-truth validation of multimodal, absolute MPI applications in the clinical setting. Its dedicated and 3D printed design enables tracer kinetic measurement, including time activity curve and potentially compartmental myocardial blood flow analysis.
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http://dx.doi.org/10.1186/s40658-022-00458-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9038974PMC
April 2022

Correction to: Development of a dedicated 3D printed myocardial perfusion phantom: proof-of-concept in dynamic SPECT.

Med Biol Eng Comput 2022 Jun;60(6):1551-1553

Robotics and Mechatronics (RaM) Group, Faculty of Electrical Engineering Mathematics and Computer Science, Technical Medical Centre, University of Twente, Enschede, The Netherlands.

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http://dx.doi.org/10.1007/s11517-022-02512-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9079028PMC
June 2022

A new colleague in nuclear medicine, the clinical technologist: quo vadis?

Eur J Nucl Med Mol Imaging 2022 Jul;49(9):3012-3015

Biomedical Photonic Imaging Group, Faculty of Science and Technology, University of Twente, Enschede, The Netherlands.

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http://dx.doi.org/10.1007/s00259-022-05789-7DOI Listing
July 2022

Evidence-based guideline of the European Association of Nuclear Medicine (EANM) on imaging infection in vascular grafts.

Eur J Nucl Med Mol Imaging 2022 Aug 4;49(10):3430-3451. Epub 2022 Apr 4.

Department of Vascular Surgery and Kidney Transplantation, University of Strasbourg and GEPROVAS, Strasbourg, France.

Purpose: Consensus on optimal imaging procedure for vascular graft/endograft infection (VGEI) is still lacking and the choice of a diagnostic test is often based on the experience of single centres. This document provides evidence-based recommendations aiming at defining which imaging modality may be preferred in different clinical settings and post-surgical time window.

Methods: This working group includes 6 nuclear medicine physicians appointed by the European Association of Nuclear Medicine, 4 vascular surgeons, and 2 radiologists. Vascular surgeons formulated 5 clinical questions that were converted into 10 statements and addressed through a systematic analysis of available literature by using PICOs (Population/problem-Intervention/Indicator-Comparator-Outcome) strategy. Each consensus statement was scored for level of evidence and for recommendation grade, according to the Oxford Centre for Evidence-based Medicine criteria.

Results: Sixty-six articles, published from January 2000 up to December 2021, were analysed and used for evidence-based recommendations.

Conclusion: Computed tomography angiography (CTA) is the first-line imaging modality in suspected VGEI but nuclear medicine modalities are often needed to confirm or exclude the infection. Positron emission tomography/computed tomography (PET/CT) with 2-deoxy-2-[F]fluoro-D-glucose ([F]FDG) has very high negative predictive value but it should be performed preferably at least 4 months after surgery to avoid false positive results. Radiolabelled white blood cell (WBC) scintigraphy, given its high diagnostic accuracy, can be performed at any time after surgery.

Preamble: The European Association of Nuclear Medicine (EANM) is a professional no-profit medical association that facilitates communication worldwide between individuals pursuing clinical and research excellence in nuclear medicine. The EANM was founded in 1985. EANM members are physicians, technologists, and scientists specializing in the research and practice of nuclear medicine. The EANM will periodically define new guidelines for nuclear medicine practice to help advance the science of nuclear medicine and to improve the quality of service to patients throughout the world. Existing practice guidelines will be reviewed for revision or renewal, as appropriate, on their fifth anniversary or sooner, if indicated. Each practice guideline, representing a policy statement by the EANM, has undergone a thorough consensus process in which it has been subjected to extensive review. The EANM recognizes that the safe and effective use of diagnostic nuclear medicine imaging requires specific training, skills, and techniques, as described in each document. Reproduction or modification of the published practice guideline by those entities not providing these services is not authorized. These guidelines are an educational tool designed to assist practitioners in providing appropriate care for patients. They are not inflexible rules or requirements of practice and are not intended, nor should they be used, to establish a legal standard of care. For these reasons and those set forth below, the EANM suggests caution against the use of the current consensus document in litigation in which the clinical decisions of a practitioner are called into question. The ultimate judgement regarding the propriety of any specific procedure or course of action must be made by the physician or medical physicist in the light of all the circumstances presented. Thus, there is no implication that an approach differing from the consensus document, standing alone, is below the standard of care. To the contrary, a conscientious practitioner may responsibly adopt a course of action different from that set forth in the consensus document when, in the reasonable judgement of the practitioner, such course of action is indicated by the condition of the patient, limitations of available resources, or advances in knowledge or technology subsequent to publication of the consensus document. The practice of medicine includes both the art and the science of the prevention, diagnosis, alleviation, and treatment of disease. The variety and complexity of human conditions make it impossible to always reach the most appropriate diagnosis or to predict with certainty a particular response to treatment. Therefore, it should be recognized that adherence to this consensus document will not ensure an accurate diagnosis or a successful outcome. All that should be expected is that the practitioner will follow a reasonable course of action based on current knowledge, available resources, and the needs of the patient, to deliver effective and safe medical care. The sole purpose of this consensus document is to assist practitioners in achieving this objective.
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http://dx.doi.org/10.1007/s00259-022-05769-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9308572PMC
August 2022

Cardiac Alterations on 3T MRI in Young Adults With Sedentary Lifestyle-Related Risk Factors.

Front Cardiovasc Med 2022 22;9:840790. Epub 2022 Feb 22.

Department of Radiology, Medical Imaging Center, University Medical Center Groningen, University of Groningen, Groningen, Netherlands.

Background: Young adult populations with the sedentary lifestyle-related risk factors overweight, hypertension, and type 2 diabetes (T2D) are growing, and associated cardiac alterations could overlap early findings in non-ischemic cardiomyopathy on cardiovascular MRI. We aimed to investigate cardiac morphology, function, and tissue characteristics for these cardiovascular risk factors.

Methods: Non-athletic non-smoking asymptomatic adults aged 18-45 years were prospectively recruited and underwent 3Tesla cardiac MRI. Multivariate linear regression was performed to investigate independent associations of risk factor-related parameters with cardiac MRI values.

Results: We included 311 adults (age, 32 ± 7 years; men, 49%). Of them, 220 subjects had one or multiple risk factors, while 91 subjects were free of risk factors. For overweight, increased body mass index (per SD = 5.3 kg/m) was associated with increased left ventricular (LV) mass (+7.3 g), biventricular higher end-diastolic (LV, +8.6 ml), and stroke volumes (SV; +5.0 ml), higher native T (+7.3 ms), and lower extracellular volume (ECV, -0.38%), whereas the higher waist-hip ratio was associated with lower biventricular volumes. Regarding hypertension, increased systolic blood pressure (per SD = 14 mmHg) was associated with increased LV mass (+6.9 g), higher LV ejection fraction (EF; +1.0%), and lower ECV (-0.48%), whereas increased diastolic blood pressure was associated with lower LV EF. In T2D, increased HbA1c (per SD = 9.0 mmol/mol) was associated with increased LV mass (+2.2 g), higher right ventricular end-diastolic volume (+3.2 ml), and higher ECV (+0.27%). Increased heart rate was linked with decreased LV mass, lower biventricular volumes, and lower T values.

Conclusions: Young asymptomatic adults with overweight, hypertension, and T2D show subclinical alterations in cardiac morphology, function, and tissue characteristics. These alterations should be considered in cardiac MRI-based clinical decision making.
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http://dx.doi.org/10.3389/fcvm.2022.840790DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8902075PMC
February 2022

Patient-Tailored Approach for Diagnostics and Treatment of Mycotic Abdominal Aortic Aneurysm.

Ann Vasc Surg 2022 Jan 31. Epub 2022 Jan 31.

Departments of Surgery (Division of Vascular Surgery), Groningen, The Netherlands.

Background: The existing literature on mycotic aortic aneurysm is scarce and focuses on treatment. This study evaluates the clinical characteristics, diagnostics, treatment and outcome of patients with a mycotic abdominal aortic aneurysm treated in a tertiary referral center.

Methods: A retrospective cohort study was conducted including all patients with a proven mycotic abdominal aortic aneurysm admitted between May 2010 and July 2020. Primary outcome was mortality and secondary outcome included complications such as vascular graft/endograft infection.

Results: Twenty-four patients with a mycotic abdominal aortic aneurysm were included. Patients had a mean age of 68 ± 9 years and 20 (83%) were male. Thirteen patients (57%) had positive preoperative blood cultures. Streptococcus pneumoniae was most frequently isolated by blood culturing, pus, and vascular, or perivascular tissue cultures (17%). In 19 (83%) patients the mycotic abdominal aortic aneurysm was located infrarenally, in three (13%) patients suprarenally, and in one (4%) patient juxtarenally. Median follow-up was 20 (7-42) months. In 8 patients (33%) vascular graft and or endograft infection was diagnosed after surgical repair. Ten (42%) patients died during the follow-up period. The main causes of death were vascular graft/endograft infection-related (n = 4) and rupture of the mycotic abdominal aortic aneurysm (n = 3). No patient characteristics could be identified as predictive for mortality.

Conclusions: This study shows a large variation in presentation, diagnostic approaches, and surgical and antibiotic treatment of mycotic abdominal aortic aneurysm. The detailed information about the diagnostic approaches to this rare disease and its antibiotic and/or other treatment contributes to existing knowledge of mycotic abdominal aortic aneurysm. Because of the individual variation patients should be discussed in a multidisciplinary team with a vascular surgeon, infectious disease specialist, and clinical microbiologist.
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http://dx.doi.org/10.1016/j.avsg.2022.01.006DOI Listing
January 2022

Development of a dedicated 3D printed myocardial perfusion phantom: proof-of-concept in dynamic SPECT.

Med Biol Eng Comput 2022 Jun 19;60(6):1541-1550. Epub 2022 Jan 19.

Robotics and Mechatronics (RaM) Group, Faculty of Electrical Engineering Mathematics and Computer Science, Technical Medical Centre, University of Twente, Enschede, The Netherlands.

We aim to facilitate phantom-based (ground truth) evaluation of dynamic, quantitative myocardial perfusion imaging (MPI) applications. Current MPI phantoms are static representations or lack clinical hard- and software evaluation capabilities. This proof-of-concept study demonstrates the design, realisation and testing of a dedicated cardiac flow phantom. The 3D printed phantom mimics flow through a left ventricular cavity (LVC) and three myocardial segments. In the accompanying fluid circuit, tap water is pumped through the LVC and thereafter partially directed to the segments using adjustable resistances. Regulation hereof mimics perfusion deficit, whereby flow sensors serve as reference standard. Seven phantom measurements were performed while varying injected activity of Tc-tetrofosmin (330-550 MBq), cardiac output (1.5-3.0 L/min) and myocardial segmental flows (50-150 mL/min). Image data from dynamic single photon emission computed tomography was analysed with clinical software. Derived time activity curves were reproducible, showing logical trends regarding selected input variables. A promising correlation was found between software computed myocardial flows and its reference ([Formula: see text]= - 0.98; p = 0.003). This proof-of-concept paper demonstrates we have successfully measured first-pass LV flow and myocardial perfusion in SPECT-MPI using a novel, dedicated, myocardial perfusion phantom. This proof-of-concept study focuses on the development of a novel, dedicated myocardial perfusion phantom, ultimately aiming to contribute to the evaluation of quantitative myocardial perfusion imaging applications.
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http://dx.doi.org/10.1007/s11517-021-02490-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9079041PMC
June 2022

Toward Reliable Uptake Metrics in Large Vessel Vasculitis Studies.

Diagnostics (Basel) 2021 Oct 26;11(11). Epub 2021 Oct 26.

Department of Nuclear Medicine and Molecular Imaging, University Medical Center Groningen, University of Groningen, 9700 RB Groningen, The Netherlands.

The aim of this study is to investigate the influence of sex, age, fat mass, fasting blood glucose level (FBGL), and estimated glomerular filtration rate (eGFR) on blood pool activity in patients with large vessel vasculitis (LVV). Blood pool activity was measured in the superior caval vein using mean, maximum, and peak standardized uptake values corrected for body weight (SUVs) and lean body mass (SULs) in 41 fluorodeoxyglucose positron emission tomography/computed tomography (FDG-PET/CT) scans of LVV patients. Sex influence on the blood pool activity was assessed with t-tests, while linear correlation analyses were used for age, fat mass, FBGL, and eGFR. Significantly higher SUVs were found in women compared with men, whereas SULs were similar between sexes. In addition, higher fat mass was associated with increased SUVs (r = 0.56 to 0.65; all < 0.001) in the blood pool, but no correlations were found between SULs and fat mass (r = -0.25 to -0.15; all > 0.05). Lower eGFR was associated with a higher FDG blood pool activity for all uptake values. In FDG-PET/CT studies with LVV patients, we recommend using SUL over SUV, while caution is advised in interpreting SUV and SUL measures when patients have impaired kidney function.
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http://dx.doi.org/10.3390/diagnostics11111986DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617769PMC
October 2021

Plasma Pyruvate Kinase M2 as a marker of vascular inflammation in giant cell arteritis.

Rheumatology (Oxford) 2022 07;61(7):3060-3070

Department of Rheumatology and Clinical Immunology.

Objectives: GCA is a large vessel vasculitis in which metabolically active immune cells play an important role. GCA diagnosis is based on CRP/ESR and temporal artery biopsies (TABs), in combination with 18F-fluorodeoxyglucose ([18F]FDG)-PET/CT relying on enhanced glucose uptake by glycolytic macrophages. Here, we studied circulating Pyruvate Kinase M2 (PKM2), a glycolytic enzyme, as a possible systemic marker of vessel wall inflammation in GCA.

Methods: Immunohistochemical detection of PKM2 was performed on inflamed (n = 12) and non-inflamed (n = 4) TABs from GCA patients and non-GCA (n = 9) patients. Dimeric PKM2 levels were assessed in plasma of GCA patients (n = 44), age-matched healthy controls (n = 41), metastatic melanoma patients (n = 7) and infection controls (n = 11). CRP, ESR and macrophage markers calprotectin and YKL-40 were correlated with plasma PKM2 levels. To detect the cellular source of plasma PKM2 in tissue, double IF staining was performed on inflamed GCA TABs. [18F]FDG-PET scans of 23 GCA patients were analysed and maximum standard uptake values and target to background ratios were calculated.

Results: PKM2 is abundantly expressed in TABs of GCA patients. Dimeric PKM2 plasma levels were elevated in GCA and correlated with CRP, ESR, calprotectin and YKL-40 levels. Elevated plasma PKM2 levels were downmodulated by glucocorticoid treatment. PKM2 was detected in both macrophages and T cells at the site of vascular inflammation. Circulating PKM2 levels correlated with average target to background ratios PET scores.

Conclusion: Elevated plasma PKM2 levels reflect active vessel inflammation in GCA and may assist in disease diagnosis and in disease monitoring.
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http://dx.doi.org/10.1093/rheumatology/keab814DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9258600PMC
July 2022

Plasma Nitrate Levels Are Related to Metabolic Syndrome and Are Not Altered by Treatment with DPP-4 Inhibitor Linagliptin: A Randomised, Placebo-Controlled Trial in Patients with Early Type 2 Diabetes Mellitus.

Antioxidants (Basel) 2021 Sep 29;10(10). Epub 2021 Sep 29.

Medical Center Groningen, Department of Internal Medicine, Division of Vascular Medicine, University of Groningen, 9713 Groningen, The Netherlands.

The depletion of nitrate and nitrite, stable nitric oxide (NO) end-products, promotes adipose tissue dysfunction and insulin resistance (IR). Dipeptidyl peptidase-4 (DPP-4) inhibitors have the potentially beneficial side effect of increasing NO availability. In this study, nitrate and nitrite levels and the effects of DPP-4 inhibitor linagliptin were investigated in relation to metabolic syndrome (MetS) markers. Treatment-naive patients with early type 2 diabetes mellitus (T2DM) ( = 40, median age 63 IQR (55-67) years, 63% male, mean HbA1c 45 ± 4.4 mmol/mol) were randomized (1:1) to linagliptin (5 mg/day) or placebo. MetS-related markers (body mass index (BMI), triglycerides, HOMA-IR, gamma-glutamyltransferase (GGT), C-reactive protein (CRP), and adiponectin), plasma levels of nitrate, nitrite, total free thiols (TFT) and vegetable intake were estimated at baseline and after 4 and 26 weeks of treatment. Plasma nitrate, but not nitrite, correlated positively with vegetable intake (r = 0.38, = 0.018) and was inversely associated with HOMA-IR (r = -0.44, = 0.006), BMI (r = -0.35, = 0.028), GGT (r = -0.37, = 0.019) and CRP (r = -0.34, = 0.034). The relationship between nitrate and HOMA-IR remained significant after adjusting for BMI, CRP, vegetable intake and GGT. With stable vegetable intake, nitrate and nitrite, TFT, adipokines and CRP did not change after 26 weeks of linagliptin treatment. While plasma nitrate is inversely associated with MetS, linagliptin treatment does not significantly influence nitrate and nitrite concentrations, oxidative stress, adipose tissue function and systemic inflammation.
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http://dx.doi.org/10.3390/antiox10101548DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8533083PMC
September 2021

Balancing Speed and Accuracy in Cardiac Magnetic Resonance Function Post-Processing: Comparing 2 Levels of Automation in 3 Vendors to Manual Assessment.

Diagnostics (Basel) 2021 Sep 24;11(10). Epub 2021 Sep 24.

Medical Imaging Center, Department of Radiology, University Medical Center Groningen, University of Groningen, Hanzeplein 1, 9713 GZ Groningen, The Netherlands.

Automating cardiac function assessment on cardiac magnetic resonance short-axis cines is faster and more reproducible than manual contour-tracing; however, accurately tracing basal contours remains challenging. Three automated post-processing software packages (Level 1) were compared to manual assessment. Subsequently, automated basal tracings were manually adjusted using a standardized protocol combined with software package-specific relative-to-manual standard error correction (Level 2). All post-processing was performed in 65 healthy subjects. Manual contour-tracing was performed separately from Level 1 and 2 automated analysis. Automated measurements were considered accurate when the difference was equal or less than the maximum manual inter-observer disagreement percentage. Level 1 (2.1 ± 1.0 min) and Level 2 automated (5.2 ± 1.3 min) were faster and more reproducible than manual (21.1 ± 2.9 min) post-processing, the maximum inter-observer disagreement was 6%. Compared to manual, Level 1 automation had wide limits of agreement. The most reliable software package obtained more accurate measurements in Level 2 compared to Level 1 automation: left ventricular end-diastolic volume, 98% and 53%; ejection fraction, 98% and 60%; mass, 70% and 3%; right ventricular end-diastolic volume, 98% and 28%; ejection fraction, 80% and 40%, respectively. Level 1 automated cardiac function post-processing is fast and highly reproducible with varying accuracy. Level 2 automation balances speed and accuracy.
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http://dx.doi.org/10.3390/diagnostics11101758DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8534796PMC
September 2021

F-BMS986192 PET Imaging of PD-L1 in Metastatic Melanoma Patients with Brain Metastases Treated with Immune Checkpoint Inhibitors: A Pilot Study.

J Nucl Med 2022 06 9;63(6):899-905. Epub 2021 Sep 9.

Department of Medical Oncology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;

Immune checkpoint inhibitors (ICIs) targeting programmed cell death protein-1 (PD-1)/programmed cell death ligand-1 (PD-L1) frequently induces tumor response in metastatic melanoma patients. However, tumor response often takes months and may be heterogeneous. Consequently, additional local treatment for nonresponsive metastases may be needed, especially in the case of brain metastases. Noninvasive imaging may allow the characterization of (brain) metastases to predict response. This pilot study uses F-BMS986192 PET for PD-L1 expression to explore the variability in metastatic tracer uptake and its relation to tumor response, with a special focus on brain metastases. Metastatic melanoma patients underwent whole-body F-BMS986192 PET/CT scanning before and 6 wk after starting ICI therapy. F-BMS986192 uptake was measured in healthy tissues, organs, and tumor lesions. Tumor response was evaluated at 12 wk using CT of the thorax/abdomen and MRI of the brain. RECIST, version 1.1, was used to define therapy response per patient. Response per lesion was measured by the percentage change in lesion diameter. Toxicity was assessed according to Common Terminology Criteria for Adverse Events, version 4.0. Baseline F-BMS986192 PET/CT was performed in 8 patients, with follow-up scans in 4 patients. The highest tracer uptake was observed in the spleen, bone marrow, kidneys, and liver. Tracer uptake in tumor lesions was heterogeneous. In total, 42 tumor lesions were identified at baseline, with most lesions in the lungs ( = 21) and brain ( = 14). Tracer uptake was similar between tumor locations. F-BMS986192 uptake in lesions at baseline, corrected for blood-pool activity, was negatively correlated with the change lesion diameter at response evaluation (r = -0.49, = 0.005), both in intra- and extracerebral lesions. Receiver-operating-characteristic analysis demonstrated that F-BMS986192 uptake can discriminate between responding and nonresponding lesions with an area under the curve of 0.82. At the follow-up scan, an increased F-BMS986192 uptake compared with baseline scan was correlated with an increased lesion diameter at response evaluation. In the follow-up F-BMS986192 PET scan of 2 patients, ICI-related toxicity (thyroiditis and colitis) was detected. In this pilot study, F-BMS986192 PET showed heterogeneous uptake in intra- and extracerebral metastatic lesions in melanoma patients. Baseline F-BMS986192 uptake was able to predict an ICI treatment-induced reduction in lesion volume, whereas the follow-up PET scan allowed the detection of treatment-induced toxicity.
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http://dx.doi.org/10.2967/jnumed.121.262368DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9157735PMC
June 2022

The Association between Foot and Ulcer Microcirculation Measured with Laser Speckle Contrast Imaging and Healing of Diabetic Foot Ulcers.

J Clin Med 2021 Aug 27;10(17). Epub 2021 Aug 27.

Biomedical Photonic Imaging, University of Twente, 7522 NB Enschede, The Netherlands.

Diagnosis of peripheral artery disease in people with diabetes and a foot ulcer using current non-invasive blood pressure measurements is challenging. Laser speckle contrast imaging (LSCI) is a promising non-invasive technique to measure cutaneous microcirculation. This study investigated the association between microcirculation (measured with both LSCI and non-invasive blood pressure measurement) and healing of diabetic foot ulcers 12 and 26 weeks after measurement. We included sixty-one patients with a diabetic foot ulcer in this prospective, single-center, observational cohort-study. LSCI scans of the foot, ulcer, and ulcer edge were conducted, during baseline and post-occlusion hyperemia. Non-invasive blood pressure measurement included arm, foot, and toe pressures and associated indices. Healing was defined as complete re-epithelialization and scored at 12 and 26 weeks. We found no significant difference between patients with healed or non-healed foot ulcers for both types of measurements ( = 0.135-0.989). ROC curves demonstrated moderate sensitivity (range of 0.636-0.971) and specificity (range of 0.464-0.889), for LSCI and non-invasive blood pressure measurements. Therefore, no association between diabetic foot ulcer healing and LSCI-measured microcirculation or non-invasive blood pressure measurements was found. The healing tendency of diabetic foot ulcers is difficult to predict based on single measurements using current blood pressure measurements or LSCI.
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http://dx.doi.org/10.3390/jcm10173844DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8432122PMC
August 2021

The effects of molar activity on [F]FDOPA uptake in patients with neuroendocrine tumors.

EJNMMI Res 2021 Sep 8;11(1):88. Epub 2021 Sep 8.

Department of Nuclear Medicine and Molecular Imaging, University Medical Center Groningen, Medical Imaging Center, University of Groningen, Hanzeplein 1, 9700 RB, Groningen, The Netherlands.

Background: 6-[F]fluoro-L-3,4-dihydroxyphenyl alanine ([F]FDOPA) is a commonly used PET tracer for the detection and staging of neuroendocrine tumors. In neuroendocrine tumors, [F]FDOPA is decarboxylated to [F]dopamine via the enzyme amino acid decarboxylase (AADC), leading to increased uptake when there is increased AADC activity. Recently, in our hospital, a new GMP compliant multi-dose production of [F]FDOPA has been developed, [F]FDOPA-H, resulting in a higher activity yield, improved molar activity and a lower administered mass than the conventional method ([F]FDOPA-L).

Aims: This study aimed to investigate whether the difference in molar activity affects the [F]FDOPA uptake at physiological sites and in tumor lesions, in patients with NET. It was anticipated that the specific uptake of [F]FDOPA-H would be equal to or higher than [F]FDOPA-L.

Methods: We retrospectively analyzed 49 patients with pathologically confirmed NETs and stable disease who underwent PET scanning using both [F]FDOPA-H and [F]FDOPA-L within a time span of 5 years. A total of 98 [F]FDOPA scans (49 [F]FDOPA-L and 49 [F]FDOPA-H with average molar activities of 8 and 107 GBq/mmol) were analyzed. The SUVmean was calculated for physiological organ uptake and SUVmax for tumor lesions in both groups for comparison, and separately in subjects with low tumor load (1-2 lesions) and higher tumor load (3-10 lesions).

Results: Comparable or slightly higher uptake was demonstrated in various physiological uptake sites in subjects scanned with [F]FDOPA-H compared to [F]FDOPA-L, with large overlap being present in the interquartile ranges. Tumor uptake was slightly higher in the [F]FDOPA-H group with 3-10 lesion (SUVmax 6.83 vs. 5.19, p < 0.001). In the other groups, no significant differences were seen between H and L.

Conclusion: [18F]FDOPA-H provides a higher activity yield, offering the possibility to scan more patients with one single production. Minor differences were observed in SUV's, with slight increases in uptake of [F]FDOPA-H in comparison to [F]FDOPA-L. This finding is not a concern for clinical practice, but could be of importance when quantifying follow-up scans while introducing new production methods with a higher molar activity of [F]FDOPA.
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http://dx.doi.org/10.1186/s13550-021-00829-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8426426PMC
September 2021

Let's embrace optical imaging: a growing branch on the clinical molecular imaging tree.

Eur J Nucl Med Mol Imaging 2021 12;48(13):4120-4128

Medical Imaging Center, Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Hanzeplein 1, 9700 RB, Groningen, the Netherlands.

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http://dx.doi.org/10.1007/s00259-021-05476-zDOI Listing
December 2021

F-FDG-Uptake in Mediastinal Lymph Nodes in Suspected Prosthetic Valve Endocarditis: Predictor or Confounder?

Front Cardiovasc Med 2021 11;8:717774. Epub 2021 Aug 11.

Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Groningen, Netherlands.

Prosthetic valve endocarditis (PVE) is a serious disease affecting ~0.4% of prosthetic valve recipients per year. F-FDG-PET/CT has high sensitivity and specificity for PVE and is included as major criterion for the diagnosis in recent guidelines of the European Society of Cardiology. We addressed the question whether increased FDG-uptake in mediastinal lymph nodes could help to support the visual diagnostic assessment of PVE. In this sub-analysis of a previously published retrospective multicentre study, 160 unique patients were identified who underwent F-FDG-PET/CT for evaluation of suspected PVE. F-FDG-PET/CT was performed in adherence to the European Association of Nuclear Medicine guidelines of 2015 and scans were assessed for signs of mediastinal lymph node activity by 2 experienced nuclear medicine physicians who were blinded to clinical context. Clinical diagnosis of PVE had been established based on surgical findings or multidisciplinary consensus after a 1-year follow-up in 80 of 160 patients (50%). In total, 52 patients showed increased mediastinal lymph node activity. Mediastinal lymph node activity on F-FDG-PET/CT did not increase diagnostic accuracy when added to the visual analysis of scans for signs of PVE: : 0.118, = 0.731). After excluding patients with known confounders for F-FDG-PET/CT, namely use of Bioglue® during prosthetic valve implantation and C-reactive protein levels below 40 mg/L, mediastinal lymph node activity was still not of additional diagnostic value compared to visual analysis alone (X:0.129, = 0.723). Assessment of mediastinal lymph node activity did not improve F-FDG-PET/CT diagnostic accuracy for suspected PVE compared to visual assessment of the valve alone, as it seems to be a rather a specific finding, that might be caused by sternal wound or mediastinal infections or even by subclinical respiratory infections. Future studies might elucidate whether increased FDG active lymph nodes indicate a high-risk patient group and whether more detailed assessment of mediastinal lymph nodes could improve their additional diagnostic benefit.
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http://dx.doi.org/10.3389/fcvm.2021.717774DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8385671PMC
August 2021

VEGF-Targeted Multispectral Optoacoustic Tomography and Fluorescence Molecular Imaging in Human Carotid Atherosclerotic Plaques.

Diagnostics (Basel) 2021 Jul 7;11(7). Epub 2021 Jul 7.

Department of Nuclear Medicine and Molecular Imaging, University Medical Center Groningen, University of Groningen, 9700 RB Groningen, The Netherlands.

Vulnerable atherosclerotic carotid plaques are prone to rupture, resulting in ischemic strokes. In contrast to radiological imaging techniques, molecular imaging techniques have the potential to assess plaque vulnerability by visualizing diseases-specific biomarkers. A risk factor for rupture is intra-plaque neovascularization, which is characterized by overexpression of vascular endothelial growth factor-A (VEGF-A). Here, we study if administration of bevacizumab-800CW, a near-infrared tracer targeting VEGF-A, is safe and if molecular assessment of atherosclerotic carotid plaques in vivo is possible using multispectral optoacoustic tomography (MSOT). Healthy volunteers and patients with symptomatic carotid artery stenosis scheduled for carotid artery endarterectomy were imaged with MSOT. Secondly, patients were imaged two days after intravenous administration of 4.5 bevacizumab-800CW. Ex vivo fluorescence molecular imaging of the surgically removed plaque specimen was performed and correlated with histopathology. In this first-in-human MSOT and fluorescence molecular imaging study, we show that administration of 4.5 mg bevacizumab-800CW appeared to be safe in five patients and accumulated in the carotid atherosclerotic plaque. Although we could visualize the carotid bifurcation area in all subjects using MSOT, bevacizumab-800CW-resolved signal could not be detected with MSOT in the patients. Future studies should evaluate tracer safety, higher doses of bevacizumab-800CW or develop dedicated contrast agents for carotid atherosclerotic plaque assessment using MSOT.
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http://dx.doi.org/10.3390/diagnostics11071227DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8305003PMC
July 2021

Impact of COVID-19 on the imaging diagnosis of cardiac disease in Europe.

Open Heart 2021 08;8(2)

International Atomic Energy Agency, Vienna, Austria.

Objectives: We aimed to explore the impact of the COVID-19 pandemic on cardiac diagnostic testing and practice and to assess its impact in different regions in Europe.

Methods: The online survey organised by the International Atomic Energy Agency Division of Human Health collected information on changes in cardiac imaging procedural volumes between March 2019 and March/April 2020. Data were collected from 909 centres in 108 countries.

Results: Centres in Northern and Southern Europe were more likely to cancel all outpatient activities compared with Western and Eastern Europe. There was a greater reduction in total procedure volumes in Europe compared with the rest of the world in March 2020 (45% vs 41%, p=0.003), with a more marked reduction in Southern Europe (58%), but by April 2020 this was similar in Europe and the rest of the world (69% vs 63%, p=0.261). Regional variations were apparent between imaging modalities, but the largest reductions were in Southern Europe for nearly all modalities. In March 2020, location in Southern Europe was the only independent predictor of the reduction in procedure volume. However, in April 2020, lower gross domestic product and higher COVID-19 deaths were the only independent predictors.

Conclusion: The first wave of the COVID-19 pandemic had a significant impact on care of patients with cardiac disease, with substantial regional variations in Europe. This has potential long-term implications for patients and plans are required to enable the diagnosis of non-COVID-19 conditions during the ongoing pandemic.
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http://dx.doi.org/10.1136/openhrt-2021-001681DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8349647PMC
August 2021

Diagnostic accuracy of dynamic CZT-SPECT in coronary artery disease. A systematic review and meta-analysis.

J Nucl Cardiol 2022 Aug 4;29(4):1686-1697. Epub 2021 Aug 4.

Department of Nuclear Medicine and Molecular Imaging, Medical Imaging Center, University Medical Center Groningen, University of Groningen, Hanzeplein 1, 9700 RB, Groningen, The Netherlands.

Background: With the appearance of cadmium-zinc-telluride (CZT) cameras, dynamic myocardial perfusion imaging (MPI) has been introduced, but comparable data to other MPI modalities, such as quantitative coronary angiography (CAG) with fractional flow reserve (FFR) and positron emission tomography (PET), are lacking. This study aimed to evaluate the diagnostic accuracy of dynamic CZT single-photon emission tomography (SPECT) in coronary artery disease compared to quantitative CAG, FFR, and PET as reference.

Materials And Methods: Different databases were screened for eligible citations performing dynamic CZT-SPECT against CAG, FFR, or PET. PubMed, OvidSP (Medline), Web of Science, the Cochrane Library, and EMBASE were searched on the 5th of July 2020. Studies had to meet the following pre-established inclusion criteria: randomized controlled trials, retrospective trails or observational studies relevant for the diagnosis of coronary artery disease, and performing CZT-SPECT and within half a year the methodological references. Studies which considered coronary stenosis between 50% and 70% as significant based only on CAG were excluded. Data extracted were sensitivity, specificity, likelihood ratios, and diagnostic odds ratios. Quality was assessed with QUADAS-2 and statistical analysis was performed using a bivariate model.

Results: Based on our criteria, a total of 9 studies containing 421 patients were included. For the assessment of CZT-SPECT, the diagnostic value pooled analysis with a bivariate model was calculated and yielded a sensitivity of 0.79 (% CI 0.73 to 0.85) and a specificity of 0.85 (95% CI 0.74 to 0.92). Diagnostic odds ratio (DOR) was 17.82 (95% CI 8.80 to 36.08, P < 0.001). Positive likelihood ratio (PLR) and negative likelihood ratio (NLR) were 3.86 (95% CI 2.76 to 5.38, P < 0.001) and 0.21 (95% CI 0.13 to 0.33, P < 0.001), respectively.

Conclusion: Based on the results of the current systematic review and meta-analysis, dynamic CZT-SPECT MPI demonstrated a good sensitivity and specificity to diagnose CAD as compared to the gold standards. However, due to the heterogeneity of the methodologies between the CZT-SPECT MPI studies and the relatively small number of included studies, it warrants further well-defined study protocols.
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http://dx.doi.org/10.1007/s12350-021-02721-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9345813PMC
August 2022
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