Influence of MRI-Conditional Cardiac Pacemakers on Quality and Interpretability of Images Acquired in 1 . 5T Cardiac MRI

C l i n M e d International Library Citation: Yokoyama K, Kariyasu T, Kuhara S, Imai M, Ishimura R, et al. (2015) Influence of MRI-Conditional Cardiac Pacemakers on Quality and Interpretability of Images Acquired in 1.5-T Cardiac MRI. Int J Clin Cardiol 2:030 Received: April 10, 2015: Accepted: April 22, 2015: Published: April 24, 2015 Copyright: © 2015 Yokoyama K. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Yokoyama et al. Int J Clin Cardiol 2015, 2:2 ISSN: 2378-2951

arrhythmias, the number of patients with CIEDs will likely continue to increase [2,3].It is estimated that 50% to 75% of this increasing population of patients with CIEDs will require a magnetic resonance imaging (MRI) examination at some point after implantation [4].Given that 85% of all patients with CIEDs have one or more comorbidities, facilitating comprehensive multispecialty care is important [4,5].MRI makes the early detection of medical conditions possible and offers important advantages over other imaging technologies, including the absence of ionizing radiation, excellent soft tissue resolution, and discrimination in any imaging plane [6].MRI is recommended for the workup of many neurological, oncologic, and musculoskeletal diseases because of its unmatched ability to accurately visualize soft tissue.The presence of CIEDs, however, had been considered to be a contraindication to MRI [7][8][9][10], and device manufacturers had warned against MRI procedures for patients with such devices [11][12][13].
Recently, advances in cardiac device technology and MR-specific developments have led to the introduction of MRI-conditional CIEDs, providing more diagnostic options for patients with such devices [14].In Japan, an MRI-conditional pacemaker was introduced in October 2012, and many MRI-conditional CIEDs are currently available.Patients with such MRI-conditional CIED scan safely undergo MRI examinations under certain conditions.While many of these examinations will be non-cardiac, cardiac MRI (CMR) is being performed with increasing frequency in these patients, as it allows for unparalleled assessment of morphology, function, and viability.
CMR is considered to be useful for identifying the causes of complete atrioventricular block, which is an indication for cardiac pacemaker implantation, and the causes of ventricular tachycardia (VT) and nonsustained VT, which are important indications for ICD implantation.One of the major diseases responsible for these abnormalities is cardiac sarcoidosis.Myocardial involvement of sarcoidosis is observed more frequently in Japan than in the United States or European countries and is responsible for the majority of deaths from sarcoidosis.It has been reported in Japan that cardiac sarcoidosis accounts for approximately one-third of the cases of advanced atrioventricular block in middle-aged and elderly women [6].The diagnosis of cardiac involvement is difficult because the clinical manifestations are varied and nonspecific and the diagnostic rate with endomyocardial biopsy is low [15].Recently, CMR has been found to be useful for the diagnosis of cardiac sarcoidosis, and it is now widely employed in the clinical setting [6][7][8][9][10][11][12][13][14][15][16][17][18].CMR is also considered to be useful for the diagnosis of various types of cardiomyopathy and myocardial ischemia that may be responsible for arrhythmias [19][20][21].The present study was conducted to assess the quality and interpretability of images acquired in CMR examinations for patients with MRI-conditional pacemakers.

Study population
The subjects in this study were 12consecutive patients (7 men and 5 women, age range:50 to 78 years, mean age: 68.4 ± 8.7 years) with MRI-conditional pacemakers who underwent CMR examinations at our institution between July 2013 and December2014.This retrospective study was approved by our institutional review board, and the requirement to obtain informed consent was waived.All subjects had implanted cardiac pacemakers for the treatment of atrioventricular block or sick sinus syndrome, and CMR was performed to assess the myocardial pathologic changes associated with the underlying diseases, which included cardiac sarcoidosis, cardiomyopathies, and ischemic heart disease.The clinical profiles of the subjects are shown in Table 1.
Seven subjects had Advisa MRI Sure Scan pacemaker systems (A3SR01) consisting of the Advisa MRI implantable pulse generator (IPG) and Capture Fix MRI leads (Medtronic, Inc., Minneapolis, MN, USA), 3 subjects had Accent MRI TM pacemaker systems consisting of the Accent MRI TM IPG and Tendril MRI TM leads (St.Jude Medical, Inc., St. Paul, MN, USA), and 2 subjects had Pro MRI  pacemaker systems consisting of the Etrinsa 8 DR-T and Safio S leads (BIOTRONIKSE& Co.KG, Berlin, Germany).All pacemakers were the dual-chamber type.The IPG was implanted in the left chest in all subjects.The pacemakers were set to DOO mode (80 to 90ppm), AOO mode (80ppm), or VOO mode (60 to 100ppm) during the CMR examinations.A cardiologist and a clinical engineer with specialized training were present during all CMR examinations to deal with any unforeseeable circumstances that might arise.

CMR protocol
A 1.5-T MRI system (EXCELART Vantage TM Powered by Atlas; Toshiba Medical Systems Corporation, Otawara, Japan) and a 16-channel coil (Atlas SPEEDER Body; Toshiba) were used.The slew rate and maximum intensity of the gradient field were 200mT/m/ ms and 30mT/m, respectively.The maximum spatial magnetic field gradient of the static field was 10.435 T/m (Figures 1,2).

Fat-suppressed black blood T2-weighted imaging for the evaluation of myocardial edema
Fast Advanced Spin Echo (FASE) sequences covering the range from the cardiac base to the apex in the end-diastolic phase were used to acquire axial 2-dimensionalmultislice images in a single breath-hold with ECG gating (repetition time [TR]/echo time[TE]:1600ms/80ms, flip angle:90°, matrix:256 × 256, slice thickness:10 mm, FOV:38 × 38cm,and BBTI: 550ms).The entire heart was covered by short-axis views.

Late gadolinium enhancement (LGE) images for the evaluation of myocardial scarring and fibrosis
Inversion recovery (IR) fast field echo (FFE) sequences covering the range from the cardiac base to the apex in the end-diastolic phase were used to acquire 3-dimensional images in approximately 20 seconds during a single breath-hold with ECG gating (repetition time [TR]/echo time[TE]:5ms/2ms, flip angle:12°, matrix:128×256, slice thickness:10mm, FOV: 35×35cm, and inversion time:220-270ms [continuously adjusted]).LGE images were acquired on average 5 to 10 minutes after the intravenous administration of gadopentetate dimeglumine (Magnevist; Bayer Healthcare, Osaka, Japan) with a contrast dose of 0.1mmol/kg.The entire heart was covered by 2-and 4-chamber long-axis and short-axis views.

Image evaluation
Two readers (K.Y. and T.K.) with more than 5 years of experience with CMR reviewed all of the image data sets and evaluated the quality of the acquired images.Image quality was semiquantitatively rated using a 4-point scale (4: sufficient for clinical diagnostic purposes, 3: not sufficient, but within the allowable range, 2: not clinically acceptable, and 1: could not be evaluated).The rating scale took into account whether the artifacts from the leads or IPG or the magnetic field in homogeneity due to the pacemaker system impaired the ability to delineate the endocardial and epicardial borders in cardiac function analysis based on observation of systolic myocardial wall motion and thickening as well as the ability to visualize the signals within the left ventricular walls for the evaluation of myocardial edema, scarring, and fibrosis.The assessment also included the uniformity within the lumens of the right and left cardiac chambers and the delineation of the atrioventricular valves (mitral valve and tricuspid valve) in 4-chamber cine images.This patient underwent CMR to identify the cause of complete atrioventricular block and was diagnosed as having cardiac sarcoidosis.

A. Short-axis cine images acquired using the SSFP technique
The upper row shows diastolic images and the lower row shows systolic images.The images on the left (a,d) are at the basal level, those in the center (b,e) are at the mid level, and those on the right (c,f) are at the apical level.
Minor IPG-related off-resonance stripe artifacts in the chest wall that do not extend to the heart (arrows) are seen.The artifacts do not interfere with the ability to delineate the right ventricular and left ventricular endocardial and epicardial borders or to evaluate cardiac function.No lead-related artifacts are observed.The result is grade 4 for all segments.

B. 4-chamber cine images acquired using the SSFP technique
Image "a" shows the diastolic phase and image "b" shows the systolic phase.
Minor susceptibility artifacts with characteristic dark signal voids (arrows) are observed around the atrial and ventricular leads.The artifacts interfere slightly with the ability to delineate the tricuspid valve (grade 2), but the mitral valve (arrowhead) can be assessed (grade 3).In addition, the signal uniformity within the right and left ventricular lumens is relatively high (grade 3).
C. Short-axis fat-suppressed black blood T2-weighted images (a,b,c) and short-axis late gadolinium enhancement (LGE) images (d,e,f) Minor susceptibility artifacts with characteristic dark signal voids (arrows) are observed around the atrial and ventricular leads.The artifacts extend slightly into the septum at the basal level, but assessment within the myocardium is possible (grade 3).No artifacts are observed in the other segments (grade 4).In the LGE images, many contrast-enhanced spots are seen in the left-ventricular myocardium (arrowheads).These are considered to be lesions of cardiac sarcoidosis.This patient underwent CMR to identify the cause of complete atrioventricular block, but no obvious abnormalities were found.

A. Short-axis cine images acquired using the SSFP technique
The upper row shows diastolic images and the lower row shows systolic images.The images on the left (a,d) are at the basal level, those in the center (b,e) are at the mid level, and those on the right (c,f) are at the apical level.
Severe IPG-related off-resonance stripe artifacts are observed in the chest wall, and they extend to the anterior wall at the mid and apical levels (short arrows).
Minor susceptibility artifacts with characteristic dark signal voids (long arrows) are observed around the atrial and ventricular leads.The artifacts interfere slightly with the ability to delineate the right ventricular and left ventricular endocardial and epicardial borders and to evaluate cardiac function.The results are grade 3 for the septum at the basal level, grade 2 for all segments at the midlevel, grade 2 for the anterior wall at the apical level, and grade 3 for the septum at the apical level.For all other segments, the result is grade 4.

B. 4-chamber cine images acquired using the SSFP technique
Image "a" shows the diastolic phase and image "b" shows the systolic phase.
Minor susceptibility artifacts with characteristic dark signal voids (arrows) are observed around the atrial and ventricular leads.The artifacts interfere slightly with the ability to delineate the tricuspid valve (grade 2), but assessment of the mitral valve (arrowheads) is possible (grade 4).The signal uniformity within the right and left ventricular lumens is slightly low (grade 2).
C. Short-axis fat-suppressed black blood T2-weighted images (a,b,c) and short-axis late gadolinium enhancement (LGE) images (d,e,f) Minor IPG-related susceptibility artifacts (short arrows) are seen in the anterior and lateral walls at the basal level and mid level (the assessment result is grade 3 for all of these segments).
Minor susceptibility artifacts with characteristic dark signal voids and bright rims (long arrows) are observed around the atrial and ventricular leads.The artifacts extend slightly into the septum at the basal, mid, and apical levels, but assessment within the myocardium is possible (the result is grade 3 for all of these segments).No artifacts are observed in the other segments grade 4.

Short-axis cine images:
The clarity of the endocardial and epicardial borders, which is important for cardiac function analysis, was assessed for the left ventricular anterior, septal, inferior, and lateral walls and the right ventricular free wall at the basal, mid, and apical levels.

4-chamber cine images:
Uniformity within the right and left ventricular lumens, which can be adversely affected by degradation of image quality due to magnetic field in homogeneity, was evaluated.Moreover, delineation of the mitral valve and tricuspid valve was assessed.

Short-axis fat-suppressed black blood T2-weighted images
Short-axis LGE images: Image quality in terms of the artifacts from the leads and IPG that impaired the ability to evaluate the signals within the left ventricular walls was assessed for the left ventricular anterior, septal, inferior, and lateral walls at the basal, mid, and apical levels.

Measurement of the extent of the artifacts
For the assessment of artifacts, the extent of the artifacts caused by the IPG (depth from the chest wall surface) and the size of the artifacts caused by the leads (maximum minor-axis length of the artifact) were measured in short-axis images acquired by cine imaging, fat-suppressed black blood T2-weighted imaging, and LGE imaging.The artifacts were assessed in the areas determined based on the mutual agreement of the two readers.

Results
All of the CMR examinations were performed safely and without any unexpected incidents or complications.In all subjects, the examination was completed within 45 minutes.

Image quality
Short-axis cine images: Table 2 summarizes the scores for the clarity of the endocardial and epicardial borders of each cardiac wall.The right ventricular leads were observed along the ventricular septal wall at the basal level and mid level in all subjects, and there is no much of a difference in the presence of the artifacts.In this context, the lowest score was observed for the left ventricular septal wall at the basal level (3.5 ± 0.8) and midlevel (3.6 ± 0.7) due to the presence of artifacts from the leads.Artifacts from the IPG affected the image quality of the left anterior wall in 1 of the 12 subjects (Figure 2).The borders of the left inferior and lateral walls and the right ventricular free wall were visualized with sufficient clarity for the evaluation of cardiac function.3 summarizes the scores for the uniformity within the right ventricular lumen and the delineation of the mitral valve and tricuspid valve.The scores for the uniformity within the right and left ventricular lumens were rather poor (2.8 ± 0.7).The scores for the tricuspid valve were poor (2.3 ± 0.7), and the scores for the mitral valve showed acceptable image quality (3.3 ± 0.9).

Short-axis fat-suppressed black blood T2-weighted images: Table 4
Short-axis LGE images: Table 4 and Table 5 summarize the scores for image quality in terms of the artifacts from the leads and IPG that impaired the ability to evaluate the signals inside the left ventricular walls in short-axis fat-suppressed black blood T2weighted images (Table 4) and short-axis LGE images (Table 5).In both images, the scores for the septum at the basal level and midlevel were slightly lower than the scores for the other segments.Artifacts from the leads affected the signals in the septum at the basal level and midlevel in almost all subjects.Compared with short-axis SSFP cine imaging, however, the influence of artifacts tended to be less severe in images acquired by fat-suppressed black blood T2-weighted imaging and LGE imaging.

Measurement of the extent of the artifacts
Table 6 summarizes the extent of the artifacts caused by the IPG and the size of the artifacts caused by the leads.The artifacts from the IPG and from the leads were most severe in SSFP cine images as compared with fat-suppressed black blood T2-weighted images and LGE images.

Discussion
MRI requires a high-strength static magnetic field and powerful radiofrequency and gradient magnetic fields.These requirements are associated with both theoretical and observed risks due to their effects on CIEDs [14,22].The first risk is the induction of electrical currents.This risk results from the radiofrequency and gradient magnetic fields [23].There is concern that the induced currents could lead to rapid asynchronous pacing and associated hemodynamic compromise.The second risk is interference with device function.The static, radiofrequency, and gradient magnetic fields can all interact with the circuitry of the device.These interactions have the potential to temporarily or permanently affect device function and may result in inappropriate sensing, triggering, activation, or resetting of the device.The third risk is mechanical force [24].The static magnetic field exerts forces on certain metals.CIEDs contain small amounts of these metals, making them weakly ferromagnetic.As a result, there is a possibility that these devices may migrate when placed in the scanner because they are attracted to the magnet.A 6-week interval between device implantation and MRI examination is recommended in order to allow fibrosis encapsulation of the leads and IPG [25].The last risk is lead heating.The radiofrequency field can cause heating at the lead-myocardial interface.However, an in vivo canine study reported that heating at the lead tip was minimal when a clinical MRI protocol was used [14].It has been suggested that the cooling effect of blood flow through the heart may be a protective factor.
Despite the above concerns, several studies have demonstrated that patients with CIEDs can safely undergo MRI examinations under close supervision [26][27][28].However, nearly all CIEDs are currently considered to be a contraindication to MRI.In 2011, the Revo MRI Sure Scan pacemaker system (Medtronic, Inc.) was approved by the FDA in the United State as an MRI-conditional device, and approval of the Advisa MRI Sure Scan pacemaker system (Medtronic, Inc.) followed in 2013.In Japan, the first MRI-conditional pacemaker was the Advisa MRI Sure Scan pacemaker system, which was introduced in October 2012, and many MRI-conditional CIEDs are currently available.The term "MRI-conditional" refers to a lack of known hazards if a certain set of conditions are met.For these devices, the initial conditions included a maximum gradient slew rate of <200T/m/s, a whole-body specific absorption rate (SAR) of <2W/kg, and a head SAR of <3.2W/kg (normal operating mode).
The SSFP technique is the most widely employed scanning method in routine clinical CMR examinations.With an SSFP pulse sequence, the entire heart is typically covered by cine 2-, 3-, and 4-chamber longaxis and short-axis views.Short-axis views are most frequently used for the evaluation of chamber volumes, ejection fraction, wall motion, and myocardial remodeling.In order to evaluate these parameters in short-axis views, it is necessary to trace the endocardial and epicardial borders in the range from the base to the apex manually or semiautomatically using a workstation.The clarity of the endocardial and epicardial borders of each cardiac wall is therefore very important.
In the visual assessment of the clarity of the endocardial and epicardial borders of each cardiac wall in short-axis cine images, the scores for the left ventricular septal wall at the basal level and midlevel were relatively low due to the presence of artifacts from the leads.In addition, artifacts from the IPG affected the image quality of the left anterior wall in 3 of the 12 subjects, and the image quality was quite poor in 1 of these 3 subjects.The reason of this fact was unknown and was considered to be unrelated with body size of this subject.
In the assessment of the extent of the artifacts caused by the IPG and the size of the artifacts caused by the leads, the artifacts were found to be larger in the short-axis SSFP cine images than in the short-axis fat-suppressed black blood T2-weighted images or shortaxis LGE images.The SSFP technique is one of the most sensitive scanning methods with regard to local field in homogeneities that can occur in patients with metallic or electronic implants.Although local field in homogeneities did cause local artifacts along the leads, many MRI-conditional CIEDs incorporate modifications to ensure safety; for example, the leads are modified to reduce RF heating and the amount of ferromagnetic materials is limited.These modifications may have reduced the level of artifacts observed, but it is not possible to report proof for such mechanisms.
Schwitter et al. have reported the results of the Advisa MRI randomized clinical multicenter study to evaluate CMR image quality for SSFP cine images and tagging CMR [5].In their study, cine SSFP acquisitions yielded good to excellent image quality for the left ventricle and right ventricle in most cases, and only 5% of the left ventricular MR acquisitions and 2% of the right ventricular MR acquisitions were of nondiagnostic quality.In our study, the influence of artifacts on the cardiac walls was also localized, and the artifacts did not have a severe impact on the evaluation of cardiac function.
The results for the visual assessment of the uniformity within the right and left ventricular lumens in 4-chamber cine images were rather poor, and some deterioration attributable to magnetic field in homogeneity was observed.However, this result did not appear to affect the evaluation of cardiac function.
Regarding the delineation of the mitral valve and tricuspid valve, the scores for the mitral valve showed that it was visualized with acceptable image quality, but the scores for the tricuspid valve were poor.It is considered that artifacts along the lead running from the right atrium to the right ventricle, which were caused by local field in homogeneity, strongly affected the delineation of the tricuspid valve.
Concerning the results for image quality in short-axis fatsuppressed black blood T2-weighted images and short-axis LGE images, the scores for the septum at the basal level and midlevel were slightly lower than the scores for the other segments.Artifacts from the leads affected the signals in the septum at the basal level and midlevel in almost all subjects.Compared with short-axis SSFP cine imaging, however, the influence of artifacts tended to be less severe in images acquired by fat-suppressed black blood T2-weighted imaging and LGE imaging.
It should be noted, however, that although lead-induced artifacts in the septum at the basal level and midlevel did not present problems for the subjects in the present study, the lesions of cardiac sarcoidosis are frequently located in these areas.It is therefore expected that cases in which artifacts from the leads interfere with the diagnosis of cardiac sarcoidosis will be encountered in the future as the number of cases examined by CMR increases [6,17].
Our study has several limitations.First and most important, the number of subjects is small.A multicenter trial will be necessary for the evaluation of a substantial number of patients.Second, the visual scoring of image quality is subjective and does not permit quantitative analysis.Third, we used only a single MRI scanner and only a single type of scan sequence which we employ for routine examinations.Susceptibility artifacts are typically suppressed by reducing the TE, increasing the bandwidth, increasing the resolution in the phase direction, and employing spin echo sequences rather than gradient echo sequences.In the future, it will be necessary to develop sequences and scan parameters that reduce artifacts.However, cardiac MRI requires high temporal resolution and other stringent imaging conditions, and it may therefore be difficult to eliminate the influence of artifacts completely.

Conclusion
CMR can be performed safely in patients with MRI-conditional pacemakers, and image quality and interpretability are acceptable for the analysis of cardiac function as well as the evaluation of myocardial edema, scarring, and fibrosis, although some deterioration in uniformity within the lumens of the cardiac chambers due to magnetic field in homogeneity and artifacts from the leads and from the IPG may be observed.

Figure 2 :
Figure 2: 67-year-old woman (case 3) with a dual-chamber MRI-conditional pacemaker implanted in the left chest wall.

Table 2 :
Visual assessment scores for the clarity of the endocardial and epicardial borders of each cardiac wall in short-axis cine images

Table 3 :
Visual assessment scores for uniformity within the right and left ventricular lumens and delineation of the mitral valve and tricuspid valve in 4-chamber cine images

Table 4 :
Visual assessment scores for image quality in terms ofthe artifacts from the leads and IPG that impaired the ability to evaluate the signals inside the left ventricular walls in short-axis fat-suppressed black blood T2-weighted images

Table 5 :
Visual assessment scores for image quality in terms of the artifacts from the leads and IPG that impaired the ability to evaluate the signals inside the left ventricular walls in short-axis late gadolinium enhancement images

Table 6 :
Extent of the artifacts caused by the IPG and size of the artifacts caused by the leads • Page 6 of 7 • ISSN: 2378-2951 Yokoyama et al.Int J Clin Cardiol 2015, 2:2