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Published online before print December 10, 2004, 10.1148/radiol.2342032059
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(Radiology 2005;234:542-547.)
© RSNA, 2004


Pediatric Imaging

MR Coronary Angiography and Late-Enhancement Myocardial MR in Children Who Underwent Arterial Switch Surgery for Transposition of Great Arteries1

Andrew M. Taylor, BA, MD, MRCP, FRCR, Steven Dymarkowski, MD, PhD, Pascal Hamaekers, Reza Razavi, MBBS, MRCP, MRCPCH, Marc Gewillig, MD, PhD, Luc Mertens, MD, PhD and Jan Bogaert, MD, PhD

1 From the Departments of Radiology (A.M.T., S.D., P.H., J.B.) and Pediatric Cardiology (M.G., L.M.), Gasthuisberg University Hospital, Leuven, Belgium; Cardiothoracic Unit, Institute of Child Health and Great Ormond Street Hospital for Children, Great Ormond St, London WC1N 3JH, England (A.M.T.); and Cardiac MR Research Group, Division of Imaging Sciences, Guy’s Hospital, London, England (A.M.T., R.R.). Received December 19, 2003; revision requested February 26, 2004; revision received April 19; accepted May 24. Supported in part by a grant from the Belgian Foundation for Research in Pediatric Cardiology. A.M.T. supported by a Marie-Curie Fellowship of the European Commission. L.M. is a clinical researcher for the Fund for Scientific Research (FWO). Address correspondence to A.M.T. (e-mail: a.taylor@ich.ucl.ac.uk).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To prospectively evaluate the feasibility of magnetic resonance (MR) coronary artery imaging and to define myocardial damage with late-enhancement myocardial MR imaging in children who underwent arterial switch surgery for transposition of the great arteries.

MATERIALS AND METHODS: The local research ethics committee approved this study, and the subjects and/or a parent or guardian gave informed consent. Sixteen asymptomatic subjects who had undergone arterial switch surgery for transposition of the great arteries were studied (mean age, 10.8 years ± 1.3; 11 male subjects, five female subjects). MR coronary angiography, late-enhancement MR imaging, global ventricular function, and regional wall motion were assessed. Fifteen children were awake during imaging; one was imaged with the use of general anesthetic.

RESULTS: In 23 (72%) of 32 coronary arteries imaged, diagnostic-quality images of the coronary ostium and proximal coronary artery course were acquired; this increased to 100% in subjects older than 11 years. No coronary ostial stenoses were seen. In all subjects, the proximal course of the coronary arteries was visualized. Two subendocardial viability defects were detected, which corresponded to known compromise of the artery that supplied that territory at the time of surgery. Global left and right ventricular function were preserved, with no regional wall abnormalities.

CONCLUSION: Diagnostic-quality MR coronary angiography is feasible in subjects who have undergone arterial switch surgery for transposition of the great arteries, with no unexpected areas of myocardial infarction detected.

© RSNA, 2004


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Arterial switch surgery is now the treatment of choice for transposition of the great arteries. In this procedure, the aorta and main pulmonary artery are transected, switched, and reanastomosed to the correct ventricle. The coronary arteries and a small portion of aortic sinus are excised when the aorta is transected and are reimplanted once the aorta is connected to the left ventricular outflow tract (1). Good midterm prognosis for this surgery has been reported, with most complications and mortality occurring within the 1st year of life (2,3).

Most deaths that occur during this period are secondary to myocardial ischemia or infarction associated with relocation of the coronary arteries at surgery. However, little is known about the natural history of the coronary development in children as they grow. In general, coronary investigations are restricted to patients who have evidence of myocardial ischemia clinically or at electrocardiography, though several studies (46) have demonstrated coronary abnormalities in otherwise asymptomatic individuals. Because of issues related to repeated x-ray exposure (7,8), morbidity associated with the procedure itself, and potential toxicity of iodinated contrast agents, screening of this group of subjects with x-ray coronary angiography is not feasible.

Magnetic resonance (MR) coronary angiography has been demonstrated to be suitable for defining anomalous coronary arteries in adults (9,10) and adolescents (11) and may provide an alternative noninvasive method for following coronary changes (coronary ostial stenosis and proximal coronary artery kinking) in subjects after arterial switch surgery.

Thus, the purpose of our study was to prospectively evaluate the feasibility of MR coronary artery imaging and define myocardial damage with late-enhancement myocardial MR imaging in children who have undergone arterial switch surgery for transposition of the great arteries.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Fifty subjects 8–16 years of age who underwent arterial switch surgery for transposition of the great arteries were invited to participate in the study. The exclusion criteria included pacemaker, claustrophobia, and inability to cooperate during MR imaging. Sixteen subjects who responded to the invitation letter and fulfilled the inclusion criteria were included in the study (mean age, 10.8 years ± 1.3; age range, 8.7–14.1 years; 11 male and five female subjects). The study was performed during a 4-month period between February and May 2003. One surgeon performed 15 of the arterial switch surgeries. The local research ethics committee approved the study. The subject and/or a parent or guardian gave informed consent.

All subjects were asymptomatic at the time of MR imaging. Fifteen subjects were imaged while awake, and one subject (aged 8 years) was imaged with the use of general anesthesia. This subject was imaged for other clinical reasons (assessment of pulmonary artery anatomy after routine echocardiography revealed an increased Doppler velocity in the neopulmonary artery) but underwent coronary artery imaging as part of this study (informed consent given).

MR Imaging Protocol
MR imaging was performed with only knowledge of the subject’s clinical history of the underlying diagnosis, which necessitated arterial switch surgery for transposition of the great arteries. All images were obtained with a 1.5-T MR imager (Intera; Philips Medical Systems, Best, the Netherlands) equipped with Master gradients (amplitude of 30 mT/m, slew rate of 150 mT/m/sec) by using a dedicated cardiac software package (Release 9; Philips Medical Systems). A standard five-element synergy cardiac coil and vector electrocardiographic, or VCG, cardiac triggering were used. All subjects were examined in the supine position with the VCG leads on the anterior left hemithorax.

For all examinations, a local shim volume was positioned over the heart to optimize the magnetic field homogeneity in this region. A survey examination in three orthogonal planes was performed initially to localize the heart within the chest.

MR coronary angiography.—Standardized methods were used for performing MR coronary angiography, with data acquisition performed during middle to late diastole (12,13). MR imaging was performed during free breathing by using prospective respiratory navigator-echo gating in the subjects who were awake. In the anesthetized subject, MR images were acquired during suspended respiration for periods of 30 seconds (ventilator turned off, as controlled by the anesthetist). This was repeated over several periods of suspended respiration, with adequate rest periods between breath holds. Respiratory motion was also suspended prior to and during the navigator-echo initialization process to ensure that the navigator-echo gating window was set around the navigator-echo diaphragm position during paused ventilation.

T2 preparation and fat-saturated MR pulses were applied just prior to data acquisition to obtain high contrast between the blood and myocardium and between fat and other structures, respectively (14). Parallel imaging technology (sensitivity encoding) was used to decrease the acquisition duration of this examination by a factor of 2 (15).

Initially, low-spatial-resolution three-dimensional balanced turbo field-echo scout imaging was performed in the transverse plane to identify the right and left coronary arteries for subsequent positioning of the three-dimensional volumes used for high-spatial-resolution MR imaging. The sequence parameters were repetition time msec/echo time msec of 4/2, flip angle of 70°, section thickness of 3.5 mm, matrix of 102 x 256, and field of view of 270 mm. The high-spatial-resolution MR imaging slabs were positioned on the scout images by using a three-point "planscan tool" in the plane of the right- and left-sided coronary arteries, respectively (three-dimensional balanced turbo field echo: 5.7/2.8, flip angle of 110°, section thickness of 3.0 mm). The matrix was 272 x 272 with a field of view of 270 mm. This yielded a spatial resolution of 1.0 x 1.0 mm that was reconstructed to a matrix of 512 x 512 by means of additional zero-filling to give a spatial resolution of 0.54 x 0.54 x 1.5 mm. The three-dimensional slab consisted of 20 sections of 1.5-mm reconstructed thickness, resulting in coverage of 30 mm.

Cine MR imaging.—Balanced turbo field-echo cine MR images were acquired in the vertical long axis, horizontal long axis, and a short-axis stack, covering the entirety of both ventricles. Images were acquired in a single breath hold, with a total of 8–12 breath holds required to encompass the ventricles in the short axis. The sequence parameters were 3.8/1.9, flip angle of 60°, section thickness of 7 mm, matrix of 160 x 256, field of view of 300 mm, and temporal resolution of 30 phases.

Late-enhancement MR imaging.—Inversion-recovery contrast material–enhanced MR imaging was performed after intravenous injection of gadopentetate dimeglumine (0.2 mmol per kilogram of body weight) by using a three-dimensional T1-weighted turbo field-echo technique in the cardiac short- and long-axis planes (4.5/1.3, flip angle of 15°, section thickness of 10 mm, matrix of 128 x 256, field of view of 350 mm). The inversion time was adjusted for optimal suppression of normal myocardial signal, and the images were obtained within 10–15 minutes after injection (inversion time approximately 200–300 msec).

MR Image Analysis
MR angiography and late-enhancement MR imaging.—The MR images were transferred to a commercially available workstation (Pride; Philips Medical Systems). Maximum intensity projections along the course of the right and left coronary arteries were created with the imaging tool Soap Bubble (Philips Medical Systems) (16). These images were reviewed and defined as either diagnostic or nondiagnostic. Images were deemed diagnostic if there was clear visualization of all of the following: the coronary artery ostia, the proximal coronary artery course and any anomalies, the right coronary artery along the anterior atrioventricular groove to the inferior margin of the heart, and the left anterior descending and left circumflex arteries from their origin to the anterior interventricular groove and posterior atrioventricular groove, respectively. If any of these features were not visualized clearly, the images were deemed nondiagnostic. Two experienced cardiovascular MR observers reviewed the images independently (A.M.T. and J.B., with 5 and 10 years of experience in cardiovascular MR imaging, respectively).

The coronary artery anatomy was compared with the original surgical findings in all patients (the reference standard). Coronary artery diameters and lengths of vessels visualized were measured. Late-enhancement MR images were also reviewed independently by A.M.T. and J.B.

Ventricular volume measurements.—One observer (A.M.T.) performed the left and right ventricular measurement analysis. The end-diastolic and end-systolic images were selected by means of direct visualization and measurements performed by hand for both ventricles on the short-axis images (the papillary muscles were excluded form the volume measurements). The left and right ventricular end-diastolic volume, end-systolic volume, stroke volume, and ejection fraction were then calculated automatically. All values were corrected for body surface area (17).

The same experienced observers (A.M.T. and J.B.) independently assessed left ventricular regional wall motion by using a standard 17-segment frame of reference (18). Regional wall motion was recorded as normal, mild hypokinesia, moderate hypokinesia, severe hypokinesia, or akinesia.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The mean age of the 16 subjects at the time of MR imaging was 10.8 years ± 1.3 (age range, 8.7–14.1 years; 11 male and five female subjects). Mean age at surgery was 13.1 days ± 7.6; age range was 3–31 days (Table 1).


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TABLE 1. Descriptive Data for the Subject Population

 
There was complete agreement between the observers for the findings on the MR images, evidence of myocardial late enhancement, and regional wall motion analysis.

Diagnostic versus Nondiagnostic Images
Diagnostic-quality images were acquired in 23 (72%) of 32 coronary arteries imaged. No coronary ostial stenoses or proximal coronary artery kinking was identified in these subjects (Fig 1). In nine awake subjects, MR images were diagnostic for both the left- and right-sided coronary arteries. Diagnostic images for both coronary systems were acquired in all subjects aged at least 11 years (n = 7).



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Figure 1a. Maximum intensity projections reconstructed from three-dimensional MR coronary angiograms (5.7/2.8, flip angle of 110°, matrix of 272 x 272, reconstructed to an image resolution of 0.54 x 0.54 x 1.5 mm). Images show normal coronary ostia in (a) right coronary artery (oblique sagittal plane, arrow) and (b) left coronary artery system (oblique transverse plane, arrowhead).

 


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Figure 1b. Maximum intensity projections reconstructed from three-dimensional MR coronary angiograms (5.7/2.8, flip angle of 110°, matrix of 272 x 272, reconstructed to an image resolution of 0.54 x 0.54 x 1.5 mm). Images show normal coronary ostia in (a) right coronary artery (oblique sagittal plane, arrow) and (b) left coronary artery system (oblique transverse plane, arrowhead).

 
Diagnostic-quality images were acquired in the anesthetized subject. In three subjects, the right coronary artery images were of diagnostic quality, but the high-spatial-resolution left coronary artery images were nondiagnostic in one case and not acquired in two cases. In these latter two cases, difficulty in maintaining the patients’ end-expiratory diaphragm position within the navigator-echo gating window led to MR imaging being abandoned because of time constraints. In three subjects, nondiagnostic images of both coronary arteries were acquired, though MR imaging was completed in all three subjects (Fig 2). These three subjects were the youngest, second youngest, and fifth youngest within the awake group (aged 8.6, 9.1, and 10.1 years, respectively).



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Figure 2. Maximum intensity projection reconstructed from three-dimensional MR coronary angiogram (5.7/2.8, flip angle of 110°, matrix of 272 x 272, reconstructed to an image resolution of 0.54 x 0.54 x 1.5 mm). Nondiagnostic-quality image of right coronary artery (oblique sagittal plane, arrow) in an awake 8-year-old subject. Comparison should be made with appearance of right coronary artery (arrow) in Figure 3b from an anesthetized 8-year-old subject.

 
Coronary Arteries
In all 16 subjects, MR coronary angiography was used to identify the origin and course of the proximal coronary arteries correctly, as compared with surgical findings. There were 13 normal arrangements and three coronary anomalies. In two cases of anomalous coronary anatomy, the left circumflex artery arose from the right coronary artery and passed by way of a retroaortic route to the posterior atrioventricular groove. In the third case, there was a large dominant accessory left anterior descending artery arising from a common origin with the right coronary artery anteriorly (second left anterior descending artery arising normally from the left main coronary artery) (Fig 3).



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Figure 3a. Maximum intensity projections reconstructed from three-dimensional MR coronary angiograms (5.7/2.8, flip angle of 110°, matrix of 272 x 272, reconstructed to an image resolution of 0.54 x 0.54 x 1.5 mm). (a) Oblique sagittal view demonstrates anomalous origin of left circumflex artery (arrowhead) from right coronary artery (arrow). (b) Coronal view demonstrates anomalous accessory left anterior descending artery (arrowhead) arising from same ostia as right coronary artery (arrow). No ostial stenoses or proximal coronary artery kinking is seen.

 


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Figure 3b. Maximum intensity projections reconstructed from three-dimensional MR coronary angiograms (5.7/2.8, flip angle of 110°, matrix of 272 x 272, reconstructed to an image resolution of 0.54 x 0.54 x 1.5 mm). (a) Oblique sagittal view demonstrates anomalous origin of left circumflex artery (arrowhead) from right coronary artery (arrow). (b) Coronal view demonstrates anomalous accessory left anterior descending artery (arrowhead) arising from same ostia as right coronary artery (arrow). No ostial stenoses or proximal coronary artery kinking is seen.

 
Coronary artery lengths and diameters measured from the source MR images are given in Table 2. The coronary artery diameter measurements in our study population are similar to those measured at echocardiography for the left main coronary artery (mean diameters, 2.7 mm and 2.6 mm, respectively) and left anterior descending arteries (mean diameters, 2.1 mm and 2.1 mm, respectively) but are larger for the right coronary artery (mean diameters, 2.5 mm and 2.1 mm, respectively) (19).


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TABLE 2. Coronary Artery Lengths and Diameters

 
Myocardial Late Enhancement
In two subjects, an area of lateral basal left ventricular wall subendocardial late enhancement was identified. In one patient, the left circumflex coronary artery, which had been occluded at or soon after the original surgery, was not visualized at MR imaging. The appearances are consistent with myocardial infarction in the left circumflex arterial territory, which had been diagnosed previously. In the other subject, a small embolism to the left circumflex arterial territory at the time of reconstructive surgery was thought to have occurred (Fig 4). In both of these subjects, regional wall thickening was preserved in the region of the subendocardial infarction. No other late-enhancement MR abnormalities were identified.



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Figure 4. Short-axis late-enhancement MR image obtained in a patient with known left circumflex artery subendocardial infarction (4.5/1.3, flip angle of 15°, section thickness of 10 mm, matrix of 128 x 256, field of view of 350 mm). Subendocardial area of high signal intensity (arrows) is seen in lateral wall at base of heart, consistent with area of myocardial infarction, secondary to presumed coronary artery embolus at coronary ostial surgery.

 
Ventricular Function
Biventricular function was normal (left ventricle, mean of 70% ± 5 and range of 59%–77%; right ventricle, mean of 68% ± 7 and range of 58%–77%; Table 3). No regional wall motion abnormalities were identified.


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TABLE 3. Ventricular Parameters for All Subjects Normalized for Body Surface Area (n = 16)

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Arterial switch surgery is now the treatment of choice for anatomic correction of transposition of the great arteries (2,3). Complications in subjects undergoing this procedure most commonly result from myocardial ischemia or infarction, secondary to the necessary reimplantation of the coronary arteries. Although most of these problems occur in the 1st year of life, there remains concern that there will be lack of coronary ostia growth over time, with possible progression to coronary ostial stenosis or kinking of the proximal coronary arteries. In general, myocardial ischemia is only investigated in patients who present with symptoms or have alterations at routine electrocardiography. However, three x-ray angiography studies (46) have demonstrated that coronary abnormalities can be present in asymptomatic individuals (3%–7%).

In all probability, these subjects remain asymptomatic because of extensive collateral formation (4). Long-term follow-up with x-ray fluoroscopic coronary catheterization is not an option for this group of patients because of the risks of excessive radiation exposure from repeated investigations (7,8). Thus, direct noninvasive coronary artery imaging or indirect assessment of coronary artery function with either myocardial viability imaging (to assess evidence of myocardial infarction) or myocardial perfusion imaging (to assess myocardial ischemia) is required.

In the present study, we demonstrated that coronary artery imaging is possible in young patients (aged 8–14 years). Diagnostic-quality MR images of the coronary ostia and proximal coronary arteries were acquired in 72% of the coronary arteries imaged. Furthermore, for awake subjects older than 11 years, diagnostic-quality images were acquired in both coronary arteries in all subjects. We were able to identify coronary anatomy as normal or anomalous in all patients, and in those with good-quality MR images, we saw no evidence of ostial coronary stenoses or proximal coronary artery kinking.

In younger patients (aged 8–11 years), coronary images were more often not of diagnostic quality, probably because of a combination of lack of patient cooperation (movement within the imager) and rapid respiratory and cardiac rates. This group of patients may benefit from a degree of sedation prior to MR imaging, or, if clinically indicated, imaging can be performed with the use of general anesthesia. We used general anesthesia in the examination of an 8-year-old boy.

In this subject, the MR images were acquired by using navigator-echo gating, with suspended respiration for periods of 30 seconds (ventilator turned off, as controlled by the anesthetist). Thus, MR coronary angiography data were acquired with the same respiratory position for most of the examination. Although such a method of acquiring images has been described for multiple breath-hold acquisitions in awake adults (22,23), we are unaware of this method being described for MR imaging in an anesthetized child. This method enabled the acquisition of diagnostic-quality MR images in this young subject.

Late-enhancement MR imaging has now been shown to be an accurate method of sizing areas of myocardial damage in adults with ischemic heart disease (24,25) and cardiomyopathy (26,27). In combination with wall motion studies, hibernating myocardial areas that may benefit from revascularization can be identified (28). Surgical revascularization or angioplasty are therapeutic options for coronary lesions in infants and children (2931), and an assessment of myocardial viability and wall motion may help identify subjects who may benefit from treatment.

To date, the feasibility of assessing myocardial viability has been demonstrated with positron emission tomography (PET) at rest (32,33). In all asymptomatic patients, with no evidence to suggest myocardial infarction, PET images acquired at rest were normal (32,33). In patients with clinical evidence of myocardial infarction in the study of Rickers et al (34), myocardial damage was identified in all but one of the children investigated with PET.

In our own study, we identified two subjects with an area of subendocardial infarction that were not associated with any myocardial wall motion abnormality. One patient was known to have an occluded left circumflex artery at or soon after surgery, and the left circumflex artery was not identified at MR coronary angiography. The second patient was known to have a defect at resting PET in the lateral wall basally, which was presumed secondary to a small left circumflex territory embolism at the time of left coronary ostial reconstructive surgery. Thus, although numbers remain limited, PET and MR data suggest that in subjects surviving beyond the 1st year of life, there seems to be little evidence for large areas of unrecognized myocardial damage secondary to arterial switch surgery. The role for late-enhancement MR imaging would therefore be imaging in symptomatic subjects who develop either new symptoms or electrocardiographic changes.

The major limitation of our study is the lack of alternative imaging modalities to assess the accuracy of our MR data: x-ray angiography for the assessment of coronary stenoses and myocardial perfusion for the assessment of late-enhancement defects. The coronary artery course was compared with surgical findings, which confirmed the normal or anomalous course in all subjects. This was a feasibility study performed to demonstrate that good-quality MR images can be obtained in children. The ability of MR coronary angiography to accurately demonstrate proximal stenoses (13) and proximal coronary course (911) has been documented. Furthermore, in the present feasibility study, we did not feel that x-ray angiography and/or nuclear scintigraphy were warranted in our asymptomatic subjects.

A second limitation of the current study was the lack of time in which to perform rest and stress MR perfusion imaging. In our own clinical practice, we have performed MR coronary angiography, wall motion analysis, rest and stress MR perfusion imaging, and late-enhancement MR imaging within 1 hour, but this is only possible in very cooperative or anesthetized subjects. Further, large-scale studies of MR perfusion are required in subjects who have undergone arterial switch surgery.

In conclusion, we have demonstrated that diagnostic-quality MR coronary angiography is feasible in young subjects who have undergone arterial switch surgery for transposition of the great arteries, with no detection of unexpected areas of myocardial infarction. MR images were acquired without sedation or the need for breath holding in patients older than 11 years. Although images were generally not of diagnostic quality in the younger children, we demonstrated that diagnostic-quality images can be acquired with the use of general anesthesia with intermittent suspended ventilation in a single subject. We demonstrated that there were no unexpected areas of myocardial infarction, suggesting that patients who survive to this age did not have asymptomatic episodes of myocardial damage at the time of surgery. In the two patients with myocardial damage, the lesions were subendocardial in nature, with maintained wall motion and known abnormalities of the coronary artery that supplied that territory.

Performance of larger-scale cardiac MR comparative studies now seems appropriate. The combination of MR coronary angiography, MR wall motion imaging, MR perfusion, and MR viability imaging should enable accurate monitoring of asymptomatic individuals and those with symptoms or electrocardiographic changes. Such a long-term study in asymptomatic individuals may demonstrate that coronary artery complications are not the long-term problem that many have foreseen.


    FOOTNOTES
 
Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, A.M.T.; study concepts, A.M.T., S.D., L.M., J.B.; study design, A.M.T., S.D., P.H., L.M., J.B.; literature research, A.M.T.; clinical studies, A.M.T., S.D., P.H., J.B.; data acquisition, A.M.T., S.D., P.H., R.R., J.B.; data analysis/interpretation, A.M.T., J.B.; statistical analysis, A.M.T.; manuscript preparation, A.M.T., J.B.; manuscript definition of intellectual content, A.M.T., S.D., L.M., J.B.; manuscript editing, A.M.T.; manuscript revision/review, S.D., M.G., R.R., L.M., J.B.; manuscript final version approval, all authors


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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