Radiol Oncol 2024; 58(3): 313-319. doi: 10.2478/raon-2024-0053 313 review Subdiaphragmatic activity-related artifacts in myocardial perfusion scintigraphy Anja Strok1, Barbara Guzic Salobir1, Monika Stalc1,2, Katja Zaletel1,2 1 Division of Nuclear Medicine, University Medical Centre Ljubljana, Ljubljana, Slovenia 2 Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia Radiol Oncol 2024; 58(3): 313-319. Received 8 June 2024 Accepted 21 June 2024 Correspondence to: Assist. Prof. Monika Štalc, M.D., Ph.D., Division of Nuclear Medicine, University Medical Centre Ljubljana, Zaloška cesta 7, SI-1000, Slovenia. E-mail: monika.stalc@kclj.si Disclosure: No potential conflicts of interest were disclosed. This is an open access article distributed under the terms of the CC-BY license (https://creativecommons.org/licenses/by/4.0/). Background. Myocardial perfusion imaging (MPI) with single photon emission computed tomography is an estab- lished non-invasive technique for assessing myocardial ischemia. This method involves the intravenous administration of a radiopharmaceutical that accumulates in the heart muscle proportional to regional blood flow. However, image quality and diagnostic accuracy can be compromised by various technical and patient-related factors, including high non-specific radiopharmaceutical uptake in abdominal organs such as the stomach, intestines, liver, and gall- bladder, leading to subdiaphragmatic artifacts. These artifacts are particularly problematic for evaluating inferior wall perfusion and often necessitate repeated imaging, which decreases gamma camera availability and prolongs imaging times. Conclusions. Despite numerous investigated techniques to reduce interfering gastrointestinal activity, results have been inconsistent, and current MPI guidelines provide scant information on effective procedures to mitigate this is- sue. Based on our experience, some possible approaches to reducing artifacts include choosing stress testing with an exercise stress test, when possible, late imaging, fluid intake, and consuming carbonated water immediately before imaging. Key words: myocardial perfusion imaging; artifacts, subdiaphragmatic activity; single photon emission computed tomography; intervention Introduction Myocardial perfusion imaging (MPI) with single photon emission computer tomography (SPECT) is an established non-invasive imaging modality for evaluating myocardial ischemia. It is based on the intravenous application of a radiopharmaceutical that accumulates in the heart muscle in proportion to the regional blood flow.1,2 The radioactive isotope emits energy in the form of gamma rays (photons), which are detected by a tomography gamma camera approximately one hour after the application of the radiopharmaceu- tical. The data on the intensity of the accumulation of the radiopharmaceutical in the heart muscle is converted into images by the computer. Thus, scin- tigrams are generated to assess blood flow to the heart muscle during stress (exercise or pharmaco- logical) and at rest.1,2 The quality of the visual and quantitative anal- ysis of MPI images is influenced by many techni- cal and patient-related factors.3,4 Some limitations arise directly from the characteristics of the radi- opharmaceuticals. They exhibit high unspecific uptake in the abdominal organs (stomach, intes- tines, liver, and gallbladder), which can create ar- tifacts.1-3 Subdiaphragmatic activity is one of the most prevalent artifacts in SPECT imaging3,4, often interfering with the evaluation of inferior wall per- fusion in approximately 10–50% of cases.5 Radiol Oncol 2024; 58(3): 313-319. Strok A et al. / Reducing the subdiaphragmatic activity314 Artifacts in the inferior myocardial wall caused by subdiaphragmatic activity present a significant challenge by diminishing image quality and the diagnostic accuracy of the study. This can lead to suboptimal or even inadequate patient manage- ment.3 In daily practice, abdominal activity inter- ference often necessitates repeated imaging for some patients, which limits gamma camera avail- ability, prolongs imaging times, and increases ra- diation exposure for both personnel and patients in the waiting room. Currently, there is no standard approach to determine which technique(s) are most effective in reducing interfering subdiaphragmatic activ- ity. Multiple techniques have been investigated to reduce interfering gastrointestinal activity while waiting for imaging, but results have been incon- sistent. In MPI guidelines, information about pro- cedures to reduce intestinal and liver activity is scarce. In this review, we describe the effect of differ- ent interventions on subdiaphragmatic activity in MPI. Subdiaphragmatic artifacts on myocardial perfusion imaging The radiopharmaceutical used for MPI consists of a radioactive isotope of tehnecium-99m (99mTc) bound to a tetrofosmin or sestamibi molecule, which binds irreversibly to viable myocytes. In ad- dition to the heart, radiopharmaceuticals used for MPI also accumulate in other organs and tissues. Initially, they localize in the liver due to their high lipophilicity and are then excreted via the hepa- tobiliary system into the duodenum. From there, tracer activity will move distally in the small bow- el, or it may reflux into the stomach. Radiotracer can also accumulate in the gastric mucosa by ac- tive transport and retention in mitochondria or as a result of the dissociation of a tracer molecule and uptake of free 99mTc-pertechnetate.3,6,7 This subdiaphragmatic radioactivity accumulation in the immediate vicinity of the heart causes arti- facts, which interfere with the correct assessment of perfusion in the heart muscle, most often in the inferior wall of the left ventricle. In rare cases, such as with a hiatal hernia, the lateral wall can also be affected.3 Artifacts can cause either apparent increased or decreased activity in the adjacent inferior wall of the left ventricle, leading to false-negative or false- positive inferior wall perfusion defects, thereby mimicking ischemia, or concealing true perfusion defects.3,4,8 Scatter radiation from the radiotracer, combined with the effect of volume averaging, can create the appearance of increased perfusion in the inferior myocardial wall, which might mask a true perfu- sion defect in this region. On the other hand, scat- tering or superimposition of subdiaphragmatic activity on the inferior myocardial wall may cause normalization problems throughout the remain- der of the left ventricle, resulting in the appearance of relatively low activity and simulating an exten- sive perfusion defect.3,4 In clinical practice, the most common way of evaluating interfering extracardiac artifacts is vis- ually on reconstructed SPECT images (Figure 1). When the interfering activity could result in ei- ther a significant overestimation or underestima- tion of uptake in the myocardium, scans are nor- mally repeated after 0.5–1 hour. For study purposes, the intensity of interfer- ing artifacts can be visually scored using a grad- ing scale, similar to the one used previously by Albuitahi et al.9 and Bresser et al.8. The grading scale ranges from 0 to 3: 0 for absent subdiaphragmatic activity, 1 for mild subdiaphragmatic activity with no impact on visual interpretation, 2 for moderate subdiaphragmatic activity with a significant effect on interpretation, and 3 for severe subdiaphrag- matic activity leading to a substantial impact on interpretation. Moderate and severe subdiaphrag- matic tracer activity is considered relevant for the interpretation of MPI scans. Artifacts can also be analyzed semi quantita- tively on raw planar scintigrams by calculating the ratio between the myocardial and extracardiac ac- tivity (MYO:EXT ratio), a metric that has been well- studied and validated in multiple previous inves- tigations.8,10-14 The MYO:EXT ratio compares the inferior wall of the left ventricle myocardium to the infra-cardiac region10,11 and correlates strongly with the level of activity interfering with image in- terpretation or, as mentioned before, visual grad- ing.10 Because this method is time-consuming, it is mainly used for academic purposes and not in routine clinical practice. The method of obtaining this ratio is shown in Figure 2. Type of stress testing and subdiaphragmatic artefacts The frequency and intensity of the interfering extracardiac activity are affected by the patient’s Radiol Oncol 2024; 58(3): 313-319. Strok A et al. / Reducing the subdiaphragmatic activity 315 physiological characteristics as well as the type of test performed. It is well-known that subdiaphrag- matic activity is higher after vasodilator stress test- ing compared to exercise stress due to increased hepatic and gastrointestinal blood flow.1,7,10 Therefore, whenever the patient can achieve a sufficient level of exercise and has no contraindi- cations, a stress study on the bicycle or treadmill is a preferred method. In patients who are unable to exercise or achieve sufficient exercise workload, or who have complete left bundle branch block or a predominantly electro systolic rhythm with a pacemaker implanted, pharmacological stress with vasodilators is used. Regadenosone is the most commonly used pharmacologic agent for stress testing in many centres, while dipyridamole and adenosine are less common.1,2 Vasodilators induce myocardial hyperaemia in- teracting with adenosine receptors. Regadenosone is a highly specific adenosine A2A receptor agonist that induces coronary vasodilation. Adenosine and dipyridamole are less specific agents and they also stimulate the A1, A2B, and A3 adenosine recep- tors.1,4 For that reason and because only about 5% of the cardiac output goes into the myocardial vas- culature and the majority of the radiopharmaceu- tical distributes into other organs and tissues7, vas- odilators provoke known and unwanted adverse effects1, such as depressed activity and conduction of the sinoatrial and atrioventricular nodes and possible atrioventricular heart block (receptor A1), peripheral vasodilation and hypotension (receptor A2B), and bronchoconstriction which can lead to severe and life-threatening events (receptor A3).2,4 By promoting peripheral vasodilatation and dila- tation of the splanchnic vasculature, pharmacolog- ical stress test leads to more pronounced accumu- lation of radiopharmaceuticals in the abdominal organs compared to exercise stress.1,3,4,10 Due to established facts, the addition of low- level exercise along with the vasodilator stress is recommended practice in guidelines. It minimizes artifacts by increasing skeletal muscle blood flow and reducing splanchnic blood flow to the vis- cera.1,2,4,15,16 Combining the two methods results in improved image quality.2 Additionally, the com- bination of a vasodilator with a low-level exercise protocol tailored to the abilities of the individual patient helps significantly reduce vasodilator- induced side effects (flushing, dizziness, nausea, headache, hypotension).1 Based on our experience (unpublished data), approximately 60% of the patients require a phar- macological stress test, and even 80% of the sub- FIGURE 1. Interfering subdiaphragmatic activity (yellow arrow) on short and vertical long axis images of the left ventricle with (upper raw) and without attenuation correction (lower raw). Radiol Oncol 2024; 58(3): 313-319. Strok A et al. / Reducing the subdiaphragmatic activity316 jects during the COVID-19 epidemic in the years 2020–2022. The use of pharmacologic stress testing has in- creased due to factors such as poor physical per- formance, general frailty and musculoskeletal con- ditions that hinder walking.17 Furthermore, in re- sponse to the COVID-19 pandemic, the American Society of Nuclear Cardiology and the Society of Nuclear Medicine and Molecular Imaging issued recommendations aimed at reducing viral ex- posure risk for healthcare workers and patients. These guidelines highlight the importance of min- imizing interaction time and maximizing physical distancing. To reduce droplet exposure to exer- cise staff and limit close contact, pharmacologi- cal stress protocols using vasodilator agents have been preferred.18 Technical aspects of minimizing subdiaphragmatic artifacts Subdiaphragmatic artifacts can be reduced to some extent by the usage of iterative reconstruc- tion methods during processing or attenuation correction.1,19 Attenuation correction methods can be based on traditional line-source transmission or CT- based with attenuation maps in novel SPECT/CT systems and are most useful for correcting arti- facts due to soft tissue attenuation (originating from the breast or left hemidiaphragm). While a substantial number of artifacts can be corrected with these methods, but a few may also arise with their use.4 Scatter effects may be more pronounced on attenuation-corrected images.19 The use of iterative reconstruction methods has been recommended to minimize artifacts related to extracardiac activity. The iterative process is well suitable to include physical effects, such as photon attenuation and contributions from photons scat- tered in the patient. Because iterative techniques have been demonstrated to produce superior im- age reconstructions, they are preferred over tradi- tional filtered-back projections (FBP).1 Prominent infracardiac activity can result in apparent de- creased activity in the adjacent myocardium due to the reconstruction algorithm used in FBP. This is because relatively large streaks of negative num- bers due to the ramp filter pass through the heart region and thus reduce the counts.1,3 This leads to artefactual decreased activity adjacent to hot ob- jects. The phenomenon worsens with greater the subdiaphragmatic activity.3 Cardiac perfusion images are usually obtained with the patient in the supine position. Studies have demonstrated that in the presence of an infe- rior wall artifact in the stress supine MPI, a posi- FIGURE 2. An example of manually drawn regions of interests (ROIs) over the midportion of the inferior wall of the myocardium and the adjacent underlying abdominal regions on multiple projections on raw planar images of the stress study. After pixel counts were obtained for every ROI, the mean myocardial and extracardiac counts were used to calculate the ratio of myocardial to extracardiac activity (MYO:EXT ratio). Radiol Oncol 2024; 58(3): 313-319. Strok A et al. / Reducing the subdiaphragmatic activity 317 tional change (prone imaging) can be an effective technique to eliminate common artifacts. Altering the standard patient position can help overcome not only attenuation artifacts but also interfer- ing with external activity by lowering of the dia- phragm and displacing abdominal organs away from the inferior myocardial wall.1,4,20 In a few patients, duodenogastric reflux is ob- served, which can affect the quality of the scans. To alleviate the refluxed activity, some suggest positioning the patients lying on their right-hand side for 20 minutes.10 Impact of food and liquid intake The most common techniques used to reduce in- terfering activity involve the administration of food or liquids between injection and imaging. This is done to either stimulate hepatobiliary clear- ance of tracer or to distend the stomach and push the bowel loops inferiorly, further from the myo- cardium (volume effect). Techniques such as con- suming a fatty meal, solid food, milk, lemon juice, carbonated beverages, plain water, or combined interventions have been explored with variable re- sults6,8,10-14,19,21,22, and currently, there is no standard approach to determining which technique is most effective in reducing the artifacts.1 A recently published randomized study did not confirm the significant effectiveness of concomi- tant drinking of lemonade and carbonated mineral water in reducing subdiaphragmatic activity.8 On contrary, one of the previous studies showed a sig- nificant reduction in subdiaphragmatic activity by using smaller amounts of carbonated beverages. The study protocol was advantageous for patients with heart or renal failure in whom the intake of water may be a problem. Because it is desirable for these patients to drink as little water as pos- sible and given that small volumes of soda water induce a greater volume expansion of the stomach compared to normal water, the use of carbonated beverages is the preferred method.11 Also, Hussain et al. demonstrated that ingestion of carbonated water significantly improved an interfering gut artifact in the majority of their patients.14 An ex- ample of the effect of carbonated water is shown on Figure 3. Peace and colleagues found no significant ef- fect of drinking water and fat milk10, while oth- ers observed a reduced accumulation of radiop- harmaceuticals in the gastrointestinal tract when combined with drinking milk and water. They hypothesized that milk stimulates liver clearance and peristaltic movement, while water reduces ac- tivity in the stomach and accelerates the transition of biliary-excreted activity along the bowel tract.19 Similarly, in a study examining the impact of multiple techniques (drinking lemon juice, wa- ter, milk or a combination of measures), milk in- take proved to be an important factor in reducing subdiaphragmatic activity, likely due in part to faster gallbladder drainage after ingesting a fatty meal.6 They also found that the quality of scinti- grams improved when drinking fluids and eating food simultaneously.21 This is in agreement with the results of an earlier study by Boz et al., where the volume effect after consuming water and a sandwich was investigated, and the usefulness of stomach fullness on extracardiac activity was demonstrated by comparing patients in fasting and non-fasting states. They increased the volume of the stomach with a combination of fluids and solid food to push the intestine caudally and thus remove intestinal artifacts further away from the myocardium.12 Impact of drugs The use of drugs that stimulate hepatobiliary clearance or gastric motility, such as erythromycin and metoclopramide, has been reviewed with var- ying results.7,10 Metoclopramide, used for treating and preventing nausea and vomiting, is known for accelerating intestinal transit but had no effect on FIGURE 3. By administering carbonated water before imaging, carbon dioxide gas may additionally expand the stomach. The upper part of the stomach adjacent to the inferior wall of the heart is mainly filled with gas instead of water. By distending the stomach, we increase the distance between the gut and the heart, thereby reducing imaging artifacts (yellow arrow). Radiol Oncol 2024; 58(3): 313-319. Strok A et al. / Reducing the subdiaphragmatic activity318 abdominal activity in MPI and was consequently not recommended for routine practice.7,23 Drugs like the antibiotic erythromycin, which mimics motilin and leads to faster gastric empty- ing, have yielded favourable results but have been studied only in small groups.7 Some have hypothesized that iodinated oral contrast could be used to absorb gamma rays emit- ted from bowel activity but came to conclusion that some reduction in infracardiac activity was probably due to the volume effect.10,24 It was reported that proton-pump inhibitors, used to reduce stomach acid production, increase the accumulation of radiopharmaceutical in the stomach wall and can jeopardize the quality of MPI scans.7 None of these interventions and data seem to have become an integral part of the imaging pro- tocol, and more recent and comprehensive studies with a larger number of patients are needed. The impact of fasting Gastrointestinal activity and related artifacts were less pronounced in patients who were fasting or had only eaten a light meal prior to examination.3 The role of late scanning One of the most important approaches to mini- mize interfering subdiaphragmatic activity is to wait an adequate amount of time between radiop- harmaceutical administration and imaging.3 Because MPI radiopharmaceuticals are cleared from the liver at a greater rate than from the heart, delaying the imaging allows physiologic clearance of the tracer from regions adjacent to the heart and has the benefit of reducing interfering hepatic ac- tivity.1,2,4,9,10,21 The recommended time interval between in- jection and acquisition for Tc99m- tetrofosmin by the manufacturer to yield the best image quality in relation to subdiaphragmatic activity is as soon as 15 minutes. However, MPI guidelines advise later post-injection acquisitions. Minimum delays of approximately 15 minutes for exercise, 30 to 45 minutes for rest, and 45 to 60 minutes for pharma- cologic stress studies are optimal. Longer delays for repeated studies (up to 2 hours) can be used when needed.1,2 The prolongation of the time between radiop- harmaceutical application and imaging improves the quality of scintigrams4,8,10, but some authors, on the other hand, warn that it can potentially lead to reconstruction artifacts due to the increase in activity in the bowel loops8,10 and consequently ad- vise early acquisition over late scanning. The impact of physical activity To our knowledge, no studies have examined the role of controlled physical activity while waiting for MPI imaging, and the value of this intervention is uncertain. Previous research has indicated that walking exercise can significantly influence gastrointes- tinal motility. For example, Noh et al. and col- leagues found that intensive walking (exceeding 3000 steps) during bowel preparation before a co- lonoscopy led to notably higher bowel cleansing scores.25 Others have shown that physical activity accelerates colonic transit times.26-28 For patients with gynaecological cancer, engaging in pre-op- erative walking was connected to a more rapid recovery of bowel function post-surgery.29 The literature also indicates that aerobic exercise can enhance intestinal motility, especially when prac- ticed consistently over several weeks.30 However, the mechanisms by which walking stimulates in- testinal motility remain unclear. Consistent with previous literature findings, we assume that adopting a similar approach might reduce artifacts by accelerating gastrointestinal peristalsis after a pharmacological stress test. This could result in a faster clearance of radiopharma- ceuticals from the gastrointestinal tract, potential- ly improving the diagnostic accuracy of the study. Our recent unpublished data from a randomized study show that the use of electronic pedometer watches encouraged patients to walk while wait- ing for imaging. However, the number of steps did not affect the occurrence or intensity of gastroin- testinal activity-related artifacts, nor did it impact the acceptance rate of scans after pharmacological stress, compared to self-paced walking. Conclusions The problem of subdiaphragmatic activity in MPI is significant, and various approaches have been tested to reduce artifacts, but none have proven effective enough to be included in the guidelines. Based on our experience, some possible approach- es to reducing artifacts include choosing stress Radiol Oncol 2024; 58(3): 313-319. 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