Nuclear Medicine Communications:
Evaluation of myocardial perfusion and function by gated single-photon emission computed tomography technetium-99m methoxyisobutylisonitrile in children and adolescents with severe congenital heart disease
Sobic-Saranovic, Dragana P.a; Pavlovic, Smiljana V.a; Jovanovic, Ida V.b; Stefanovic, Igor D.b; Artiko, Vera M.a; Djukic, Milan M.b; Obradovic, Vladimir B.a
aInstitute for Nuclear Medicine, Clinical Center of Serbia
bUniversity Children's Hospital, School of Medicine, University of Belgrade, Belgrade, Serbia
Correspondence to Dragana P. Sobic-Saranovic, MD, PhD, Institute for Nuclear Medicine, Clinical Center of Serbia, Visegradska 26, Belgrade 11000, Serbia
Tel: +381 11 36 35 352; fax: +381 11 36 15 641;
Received 19 December 2008 Revised 14 January 2009 Accepted 14 January 2009
Objectives: The value of gated single-photon emission computed tomography technetium-99m methoxyisobutylisonitrile (gated SPECT 99mTc-MIBI) in children is not yet established probably because gated SPECT 99mTc-MIBI has rarely been used in pediatric clinical and research studies. The purpose of this study was to evaluate perfusion abnormalities and left ventricular (LV) function by gated SPECT 99mTc-MIBI in children and adolescents with severe congenital heart disease (CHD).
Methods: Seventeen children and adolescents with severe CHD (11 boys and six girls, mean age 11±4 years) underwent 2-day rest–stress (11 boys) or 1-day rest (six girls) gated SPECT 99mTc-MIBI. Myocardial perfusion was evaluated by a 17-segment model with a 5-point score to derive the summed stress score, the summed rest score (SRS), and the summed difference score based on the 4D-MSPECT software results. The extent of myocardial perfusion abnormalities was also expressed as a percentage of the LV size. The 4D-MSPECT software was used to calculate LV end-diastolic volume, end-systolic volume (ESV), and ejection fraction (EF).
Results: Reversible myocardial perfusion defect was found in 7 of 11 children (64%) who underwent rest–stress gated SPECT 99mTc-MIBI. The LV segments involved were anterior, anteroseptal, anterolateral, apical and inferior. These seven children showed significantly larger perfusion abnormalities on stress compared with rest study (18±5 vs. 7±4%, P<0.01) and higher summed stress score compared to SRS (11±4 vs. 4±2, P<0.01). Children and adolescents with myocardial ischemia had significantly lower poststress EF than rest EF (53±12 vs. 59±11%, P<0.05) and significantly higher poststress ESV than rest ESV (81±24 vs. 61±25 ml, P<0.05). In six children evaluated only at rest, perfusion defects involved anterior, anteroseptal and apical, or inferolateral segments, accounting for 31±12% of LV and with SRS of 12±5. Their global LV parameters were: end-diastolic volume 118±23 ml, ESV 56±16 ml, EF 51±10%.
Conclusion: Poststress and rest-gated SPECT 99mTc-MIBI results indicate that children and adolescents with severe CHD show a range of abnormalities in myocardial perfusion and LV function, which is useful for determining functional importance of morphological malformations. Thus, gated SPECT 99mTc-MIBI provides complementary information that may guide clinical decision making in children and adolescents with severe CHD.
Congenital heart disease (CHD) is defined as a gross structural abnormality of the heart or intrathoracic great vessels which is actually or potentially of functional significance . The reported incidence of CHD varies depending on the grades of CHD included and increased ability to detect small and trivial heart abnormalities. The incidence of severe CHD that requires expert diagnosis and care is about 2.5–3 cases per 1000 live births, whereas the incidence of moderate CHD that eventually needs cardiac care is about three cases per 1000 live births .
Patients with CHD are living longer because of recent advances in cardiac diagnosis [e.g. echocardiography, magnetic resonance imaging (MRI), cardiac-gated 64-slice computed tomography, diagnostic catheterization, angiocardiography] and treatment (interventional catheterization, cardiac surgery, cardiac intensive care) [3–6]. Echocardiography, cardiac catheterization with angiocardiography, cardiac-gated 64-slice computed tomography, and MRI are mainly used for anatomical and morphological assessment of CHD.
Comprehensive functional assessment of congenital heart malformations is important for clinical management of pediatric patients, especially children with congenital abnormalities of coronary arteries or myocardial diseases, such as hypertrophic cardiomyopathy (HCM) [7,8]. These congenital abnormalities may be silent or associated with chest pain, shortness of breath, symptoms of chronic heart failure or severe arrhythmias, indicating stress-induced ischemia, infarction or myocardial damage [7–9].
Myocardial perfusion imaging by gated single-photon emission computed tomography (gated SPECT) is a useful nuclear medicine technique for simultaneous evaluation of left ventricular (LV) function and myocardial ischemia, infarction, or damage in both adult and pediatric population [10,11]. However, the value of gated SPECT in children is not yet established probably because gated SPECT is rarely used in pediatric clinical and research studies [12,13]. Therefore, the purpose of this study was to evaluate perfusion abnormalities and LV function by gated SPECT in children and adolescents with severe CHD.
From December 2006 to November 2008, 17 children and adolescents with severe CHD were referred to our institution for evaluation of myocardial perfusion and LV function by gated SPECT technetium-99m methoxyisobutylisonitrile (99mTc-MIBI). There were 11 boys and six girls (mean age 11±4 years, range 3–17). Diagnosis of CHD was based on echocardiography and/or cardiac catheterization with angiography. The sample included three children with coronary artery fistulas (CAFs), four with anomalous origin of left coronary artery (LCA) from pulmonary artery (ALCAPA), five with atrial septal defect or ventricular septal defect (ASD/VSD), and five with HCM. Those with ASD/VSD underwent surgical closure and were referred for postoperative evaluation of LV remodeling and suspected perfusion abnormalities. Children treated after gated SPECT 99mTc-MIBI were followed up between 6 months and 1 year of intervention. The study protocol was approved by the ethics committee of our institution and written consent from parents was obtained.
Eleven children underwent a 2-day rest–stress gated SPECT 99mTc-MIBI protocol with exercise stress test on ergo bicycle (endpoints: mean heart rate 183±15 beats per minute, symptoms of severe angina, or at least 2-mm ST-segment depression on ECG) . Six children underwent only 1-day rest-gated SPECT 99mTc-MIBI protocol. The reasons for not proceeding with the stress-gated SPECT 99mTc-MIBI include significant perfusion defect at rest and inability to perform exercise stress test on ergo bicycle in four children below 7 years of age and episodes of chest pain at rest with syncope in two adolescents (12 and 13 years old).
Rest-gated SPECT was performed 45 min after intravenous administration of the 9.25 MBq/kg of 99mTc-MIBI (dose range: 148–370 MBq) . Next day for the gated SPECT stress study, the same amount of 99mTc-MIBI was intravenously injected at peak exercise with stress continuing for another minute. Gated SPECT acquisition started 30 min later. Sedation was not used during acquisition except in a 3 year-old boy according to the guidelines for pediatric sedation in nuclear medicine .
Gated SPECT 99mTc-MIBI data were acquired in the supine position with the single-head SPECT γ-camera (Siemens, e.cam; Siemens Medical Solution USA Inc., Hoffman Estates, Illinois, USA) equipped with a high-resolution low-energy collimator. Sixty-four projection images over a 180° noncircular orbit were acquired. Time per projection was 15 s, matrix size 64×64, zoom was 1.45 (except in six children below 7 years of age with small hearts in whom we used zoom 1.78), and gating eight frames per cardiac cycle.
Data reconstruction and image analysis
Using the e.soft commercial software (Siemens Medical Solution USA Inc.), transaxial tomograms were generated from gated projection data, reconstructed with filtered back-projected algorithm (Butterworth filter order 5, frequency cutoff 0.4 cycle/pixel), and reoriented to obtain oblique-angle tomograms parallel to the long and short axes of the left ventricle. The reconstructed data were projected as myocardial tomographic slices in a short axis, vertical long axis, and horizontal long axis views. Gated SPECT 99mTc-MIBI data were then processed and analyzed using 4D-MSPECT software (Siemens Medical Solution USA Inc.).
Myocardial perfusion was evaluated semiquantitatively using a 17-segment model according to the European Association of Nuclear Medicine/European Society of Cardiology guidelines . A 5-point scoring system was used for the assessment of 99mTc-MIBI uptake (4 = no uptake/background only, 3 = severe reduction of uptake, 2 = moderate reduction of uptake, 1 = mild reduction of uptake, 0 = normal uptake). Thus, total scores of MIBI uptake were automatically calculated both on the rest and exercise images, namely, summed stress score (SSS), summed rest score (SRS), and summed difference score between the SSS and SRS based on 4D-MSPECT software results. The extent of myocardial perfusion abnormalities (%) was expressed relative to the LV based on polar maps. The LV end-diastolic volume (EDV), end-systolic volume (ESV), and ejection fraction (EF) were also determined by 4D-MSPECT.
SPSS 12 (Science, Chicago, Illinois, USA) software was used for statistical analysis. The difference in global LV parameters (EDV, ESV, and EF) and perfusion scores between stress and rest studies was tested using paired two-tailed Student's t-test. A P value of less than 0.05 was considered statistically significant. The results are presented as mean±standard deviation.
Reversible myocardial perfusion defects were detected in seven of 11 children and adolescents (64%) who underwent rest–stress gated SPECT 99mTc-MIBI. Two had CAF, two ALCAPA (Fig. 1), two HCM (Fig. 2), and one surgical closure of VSD (Table 1). Results of the exercise ergo bicycle test in these children are presented in Table 1. The ECG stress test was abnormal and terminated before reaching maximum heart rate in three children with reversible perfusion defects because of significant ST depression and ventricular preexcitations. Three children developed chest pain or fatigue at peak exercise but with normal ECG findings, whereas the test was inconclusive in one child. Reversible perfusion defects were found in anterior, anteroseptal, both anterolateral and apical segments and inferior segments of the LV. These seven children had significantly larger perfusion abnormalities on stress compared with rest study (18±5 vs. 7±4%, P<0.01) and a larger SSS compared with SRS (11±4 vs. 4±2, P<0.01). In addition, poststress EF was lower than rest EF, whereas stress ESV was significantly higher than rest ESV (Table 2). In four out of seven, marked transient ischemic dilatation of the LV during stress was observed (from 1.20 to 1.57). Findings on ergo bicycle stress test and gated SPECT 99mTc-MIBI were normal in two children (CAF and ASD closure with autologuous pericardial patch), whereas the remaining two had similar perfusion abnormalities on poststress and rest images without evidence of reversible ischemia.
Perfusion was evaluated at rest in six children and adolescents [two with surgical correction of ASD/VSD, two with ALCAPA (Figs 3 and 4) and two with HCM]. Perfusion defects were detected in anterior, anteroseptal and apical, or inferolateral segments, approximating 31±12% of the LV and with SRS of 12±5 (Table 3). Global LV parameters were as follows: EDV 118±23 ml, ESV 56±16 ml, and EF 51±10%.
Treatment after gated single-photon emission computed tomography and clinical follow-up
Five children were treated with surgical or interventional procedures for severe CHD from the time of gated SPECT 99mTc-MIBI assessment to this report. Two children with ALCAPA and perfusion abnormalities on gated SPECT 99mTc-MIBI (patient no. 3 in Table 1 and patient no. 1 in Table 3) underwent surgical reimplantation of LCA into aorta. One year later, they were both in stable condition without symptoms. One child with CAFs and ischemia on gated SPECT 99mTc-MIBI (patient no. 2 in Table 1) had interventional procedure for closure of fistulas. Gated SPECT 99mTc-MIBI study performed 6 months later showed no signs of reversible ischemia or perfusion abnormalities with the child in good condition without symptoms. In two children with HCM and ischemia, a cardioverter defibrillator was implanted to prevent severe arrhythmias. Both were well at the follow-up between 6 months and 1 year with no evidence of major clinical events.
We evaluated myocardial perfusion and LV function by gated SPECT 99mTc-MIBI to assess functional implications of morphological abnormalities in children and adolescents with severe CHD and suspected postsurgical myocardial damage. In the majority of examined children, gated SPECT 99mTc-MIBI revealed reversible or fixed perfusion abnormalities. Moreover, children and adolescents with reversible perfusion abnormalities showed a significant decrease in poststress EF and an increase in poststress ESV compared with the rest values. Combined with other information, our results were used for clinical management of patients with severe CHD.
To the best of our knowledge, this is the first reported study that assessed poststress LV function in children and adolescents with severe CHD. Several related factors may account for a limited use of gated SPECT 99mTc-MIBI in children, namely, widespread availability of other assessment procedures, uncertain value of gated SPECT 99mTc-MIBI in this population, and radiation exposure during SPECT acquisition. Echocardiography remains the method of choice for evaluating children with CHD. In cases of ambiguous findings, children are referred for cardiac MRI or computed tomography . Cardiac catheterization is mainly reserved for solving diagnostic dilemmas, when measurement of pressure is important, or when there is a need for intervention. Myocardial perfusion imaging by SPECT may be of value, particularly for assessing myocardial damage and ischemia associated with CHD . Furthermore, several reports have confirmed an added diagnostic and prognostic value of gated SPECT 99mTc-MIBI over myocardial perfusion SPECT alone in adults with coronary artery disease [19–21]. Similar conclusion, however, cannot be reached in children and adolescents as studies are sparse.
El-Maghraby and El-Rahman  suggested that assessing LV volumes and EF by gated SPECT 99mTc-MIBI is problematic in children because of the small LV cavity size. Indeed, we could not reliably evaluate LV volumes and EF in a 3-year-old boy because of partial volume effect, scatter of photons from the myocardial walls to the LV cavity, and small LV cavity size. In the remaining 16 participants, we were able to gather clinically relevant data although a larger zoom during the acquisition was necessary for children below 7 years of age. Thus, our study suggests that gated SPECT 99mTc-MIBI is feasible for assessing both rest and poststress LV parameters in grown-up children with suspected ischemia.
To detect ischemia with gated SPECT 99mTc-MIBI, we used exercise stress test on ergo bicycle in 11 of 17 children and adolescents according to the AHA Scientific Statement . Exercise stress test is the most appropriate form of physiologic stress that also provides additional useful information about exercise capacity and hemodynamic changes. The exercise test was terminated in three children before achieving maximum heart rate because of significant ST depression and ventricular preexcitation in line with the guidelines for the pediatric population . The remaining eight participants achieved recommended maximum heart rate during exercise stress test [23,24]. Only rest data were collected in six participants of whom two adolescents already had severe symptoms at rest, whereas four children were below 7 years of age and unable to perform exercise stress test on an ergo bicycle. As an alternative, a pharmacological stress test has been recommended for smaller children  but our experience with such a test in children is limited. We opted not to proceed with the stress test in cases of severe perfusion abnormalities at rest. Such a conservative approach seems justified as the gated SPECT 99mTc-MIBI study at rest already indicated the extent and severity of the myocardial perfusion defect.
Perfusion and left ventricular function in different congenital heart diseases
Myocardial ischemia and fixed perfusion abnormalities were found in children with an anomalous origin or course of coronary arteries (ALCAPA and CAF), in cases of HCM, and after surgical repair of ASD/VSD.
Anomalous origin of left coronary artery from pulmonary artery
In ALCAPA (Bland–White–Gerland Syndrome), LCA arises abnormally from the pulmonary artery, whereas the right coronary artery (RCA) comes out of the aorta, as usual. Consequently, LCA carries oxygen-poor blood from the pulmonary artery to the left side of the heart. More importantly, a ‘coronary steal’ occurs wherein a low blood pressure in the pulmonary artery causes blood from the abnormal LCA to flow toward the pulmonary artery instead of the heart. Both mechanisms lead to myocardial ischemia in the territory of LCA and therefore the perfusion of the segments supplied by LCA depends on a collateral flow from RCA . Associated clinical manifestations include angina-like episodes, myocardial infarction, and congestive heart failure. Myocardial abnormalities are mostly localized at the high lateral, anterior, and lateral walls [24–26].
The literature concerning the functional significance of ALCAPA evaluated by SPECT is limited to case reports mainly in adults [26–28]. Katsuragi et al.  described two adults with ALCAPA and inferoposterior perfusion defect on thallium-201 myocardial SPECT and suggested the presence of coronary steal because of large RCA and significant shunt formation. The advantage of gated SPECT 99mTc-MIBI over perfusion imaging alone is simultaneous evaluation of perfusion abnormalities and assessment of LV function. Indeed, our gated SPECT 99mTc-MIBI 2-day rest–stress study in two participants with ALCAPA revealed anterior wall ischemia and a decrease of poststress EF because of an increase in poststress ESV. In addition, the study confirmed limited perfusion in the myocardial segments typically involved in ALCAPA [26–28]. Gated SPECT 99mTc-MIBI findings were deemed important for further clinical management. The reimplantation of the LCA into the aorta was done and both children were clinically stable at 1-year follow-up.
Coronary artery fistula
CAF is an abnormal connection between one of the coronary arteries and a heart chamber or another blood vessel. Most fistulas arise from the RCA (60%) and terminate in the right side of the heart (90%), most frequently in the right ventricle followed by the right atrium and coronary sinus [30,31]. Patients are generally asymptomatic and the anomalies are discovered incidentally during catheterization . If CAF is of hemodynamic significance, patients may present with arrhythmias, chest pain, shortness of breath, or acute myocardial infraction. Since myocardial ischemia often develops during exercise, myocardial perfusion imaging demonstrates perfusion defects distal to the fistula [31,32]. The proposed mechanism is a coronary steal with diversion of blood flow into a low-resistance channel [25,33].
In our study, two children had rare fistulas arising from LCA and terminating in the right ventricle, whereas in the third case the fistula was bi-coronal, arising from both LCA and RCA and terminating in the right ventricle. The latter case had normal LV perfusion and function. In the former two children, gated SPECT 99mTc-MIBI revealed myocardial ischemia in apical, septal and inferior regions with decreased poststress EF and increased ESV. Rubbini et al.  found ischemia on SPECT 99mTc-MIBI in two of nine adults with CAF that reportedly impacted corrective surgery. In our study, the one child with ischemia on gated SPECT 99mTc-MIBI was referred for percutaneous transcatheter embolization of CAF. Six months later, he was in good condition without symptoms and the control gated SPECT 99mTc-MIBI study was normal.
Characteristics of HCM are inappropriate myocardial hypertrophy, predominantly involving the interventricular septum of nondilated LV, and hyperkinetic ventricular function. As a result of autosomal dominant inheritance, about half of the probands with HCM have affected first-degree relatives . Children with HCM are at a higher risk for sudden cardiac death than adults. Myocardial ischemia plays an important role in the mechanism of sudden death . Detection of myocardial ischemia is, thus, important for long-term outcome and prognosis of children with CHM .
Tadamura et al.  used ammonia-13 positron emission tomography in children with HCM and demonstrated an absolute reduction in myocardial blood flow after pharmacological vasodilatation in the hypertrophic septal region. Coronary flow reserve could be impaired in children with HCM even if the myocardial perfusion is normal . Among three of five children with HCM who underwent rest/stress-gated SPECT 99mTc-MIBI, two showed reversible perfusion defect with a decrease of poststress EF and marked transient ischemic dilatation indicating severe ischemia, whereas in one child a mild fixed defect was detected. The remaining two already showed perfusion abnormalities in the septal region on rest gated SPECT 99mTc-MIBI. The two children with ischemia on rest/stress-gated SPECT 99mTc-MIBI had a cardioverter defibrillator implanted to prevent ischemia-induced arrhythmias often leading to sudden death.
Atrial septal defect/ventricular septal defect
Several studies suggest good or excellent long-term results and survival after surgical ASD or VSD closure [39,40]. In contrast, arrhythmias, pulmonary hypertension, and LV dysfunction have been described as long-term sequelae of surgical closure [39–41]. Among the five children with ASD or VSD surgical closure in our study, rest/stress-gated SPECT 99mTc-MIBI showed fixed defects in inferior and septal regions in one case, probably because of perioperative myocardial infarction. Perfusion was normal in a girl with the ASD pericardial patch closure and another girl showed a mild ischemia in the septal region without impairment of LV function. The remaining two children underwent only rest-gated SPECT 99mTc-MIBI and hypoperfusion in inferolateral regions was observed. The findings suggest that gated SPECT 99mTc-MIBI may be useful for assessing the extent of myocardial impairment after surgical closure of ASD or VSD.
This study has several limitations. First, the sample size is relatively small and diverse, which prevented us from making firm conclusions as to the impact of gated SPECT 99mTc-MIBI on clinical management of children and adolescents with specific CHD. To the best of our knowledge, however, only a few published reports used this method in children with CHD, which combined have a sample size comparable with ours. Thus, 17 cases reported here add to the growing body of knowledge. Second, we were unable to systematically compare the results of gated SPECT 99mTc-MIBI with MRI because of limited access to MRI. This approach could provide more comprehensive information about the clinical relevance of severe CHD, as shown in Fig. 4. In contrast, cardiac MRI was done in three children and the results were comparable with rest-gated SPECT 99mTc-MIBI. Third, we did not perform pharmacological stress test in our study as recommended in children below 7 years of age  because of limited experience. Finally, accurate assessment of small LV volumes remains a challenge, as evident in a 3-year-old child reported here. By changing the zoom from 1.45 to 1.78 during the acquisition, it proved possible to get clinically relevant LV volumes in children below 7 years of age.
Our preliminary results indicate that evaluation of myocardial ischemia and damage by gated SPECT 99mTc-MIBI provides clinically relevant information about functional significance of morphological abnormalities in children with severe CHD. The study also shows the additive value of simultaneous evaluation of rest and poststress LV function over perfusion alone. Thus, gated SPECT 99mTc-MIBI provides complementary information that may guide clinical decision making in this population. Our results provide rationale and justify the need for larger prospective multicenter studies to establish the role of gated SPECT 99mTc-MIBI in children and adolescents with severe CHD.
This study is supported by the Serbian Ministry of Science (Grant no. 145033). Dr Sobic-Saranovic dedicates this study to Stokic S. Dobrivoje, MD, DSc, Senior Scientist at the Center for Neuroscience and Neurological Recovery, Administrative Director for Research and Chair of Research Council of Methodist Rehabilitation Center, Jackson, Mississippi, USA.
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children and adolescents; congenital heart disease; gated single-photon emission computed tomography myocardial perfusion imaging; myocardial ischemia; poststress left ventricular function
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