REVIEW ARTICLE

https://doi.org/10.5005/jp-journals-11002-0020
Newborn
Volume 1 | Issue 1 | Year 2022

Advanced Cardiac Imaging in Neonatology

Bijoy Thattaliyath1, Prashob Porayette2, Ravi Ashwath3

1–3Department of Pediatrics, University of Iowa, Iowa City, Iowa, United States of America

Corresponding Author: Ravi Ashwath, Department of Pediatrics, University of Iowa, Iowa City, Iowa, United States of America, Phone: +3193563537, e-mail: ravichandra_ashwath@yahoo.com

How to cite this article: Thattaliyath B, Porayette P, Ashwath R. Advanced Cardiac Imaging in Neonatology. Newborn 2022;1(1):74–80.

Source of support: Nil

Conflict of interest: None

ABSTRACT

Imaging of congenital heart disease (CHD) starts in the intrauterine period by fetal echocardiography. The anatomy and physiology are confirmed postnatally by transthoracic echocardiogram. However, complex CHDs require further imaging to delineate anatomy for further management and surgical intervention. Cardiac magnetic resonance imaging (MRI) and cardiac chest tomography (CT) complement the role of transthoracic echocardiogram in delineating further details of anatomy and physiology in the neonatal period. This review covers the basic sequences and terminologies used in cardiac MRI and cardiac CT. A brief description of the indications and the ideal modality of imaging is described, including the limitations of each modality of imaging.

Keywords: Cardiac, Contrast, CT, Imaging, Indications, MRI, Neonate, Radiation, TnEcho.

INTRODUCTION

We are living in an exciting era of cardiac imaging as technological advancements now allow quick and accurate non-invasive imaging of a neonatal heart. Non-invasive cardiac imaging has come a long way since 1954 when Edler and Hertz first described the use of reflected ultrasound for imaging of the heart.1 It was not until the late 1970s before M-mode echocardiography (echo) became available for clinical use in patients.2 Invasive diagnostic cardiac catheterization was still frequently used for the diagnosis of congenital heart disease (CHD). By the 1980s, two-dimensional echo and color-flow Doppler3 greatly improved the non-invasive diagnostic imaging capabilities in pediatric patients with CHD. Advancements in fetal ultrasonography made it possible to recognize CHD in utero.4 Nowadays, echo is the first-line of non-invasive imaging tool in pediatric and adult cardiology with multiple advanced features such as tissue Doppler imaging, strain imaging, speckle tracking imaging, and three-dimensional imaging.5 There are fascinating emerging techniques such as intracardiac6 and portable ultrasonography.7 In addition, the growth of neonatal hemodynamics program has allowed performance of targeted neonatal echocardiography (TnECHO) in premature infants with hemodynamic instability8 with high diagnostic concordance between trained neonatal hemodynamics specialists and pediatric cardiology.9

Computed tomography (CT) technology was developed in the early 1970s.10 Multiple software and hardware advancements, including helical imaging, multi-detector CT, and reconstruction methods, allow ultrafast imaging of the cardiac structures. In addition, low radiation makes CT an appealing imaging modality for CHD in newborns, children, and adults.11,12

Nuclear magnetic resonance (MR) was discovered in the 1940s.13,14 MR did not enter the field of clinical cardiac imaging, however, until the early 1980s.15 The initial ungated acquisition techniques were slowly replaced by electrocardiographic gating techniques resulting in improved image quality.16–18 The first injection of gadolinium in human was in 198419 soon followed by first patient series.20 Cardiac MR (CMR) is now frequently used for anatomical and functional evaluation of CHD.21 Fetal cardiovascular magnetic resonance imaging (MRI) is an upcoming and intriguing technique showing promise as a clinical diagnostic tool in the setting of CHD when the cardiac anatomy is unresolved by ultrasound or when complementary quantitative data on blood flow, oxygen saturation, and hematocrit are required to aid in management.22–25

In most developed countries, severe CHD is diagnosed during gestation allowing appropriate medical management of these critically ill newborns immediately after birth. A postnatal chest radiography and echo can often provide the necessary details for diagnosis and management planning of neonate with CHD. When echo cannot provide the comprehensive details of relevant cardiovascular anatomy, advanced non-invasive cardiac imaging techniques such as CT and CMR play an important complementary role. Invasive diagnostic catheterization is reserved exclusively for neonates with complex cardiac anatomy needing further clarification of cardiac structures or direct measurement of pressure or oxygen saturation. This review focuses on the indications, techniques, and safety of non-invasive advanced cardiac imaging in neonates.

GOALS OF ADVANCED NEONATAL CARDIAC IMAGING

The cardiac morphology and physiology play a critical role in the clinical decisions regarding surgical or interventional palliation in neonates with CHD. A segmental approach26,27 is used to delineate cardiac anatomy from images obtained from echo and advanced imaging modality. The physiologic status is assessed using physical examination, chest radiography, echo, advanced imaging, and if needed cardiac catheterization.

INDICATIONS FOR NEONATAL CARDIAC MRI AND CT

The indication for advanced neonatal cardiac CT or CMR could be the assessment of intra-cardiac anatomy or extra-cardiac vasculature. Intra-cardiac assessment can be performed in patients with unusual complex CHD,11,12,28 cardiac tumors,29 cardiomyopathy30 or to help decide single vs biventricular repair in patients with borderline ventricular hypoplasia.31 Extracardiac indications include the assessment of vascular structures,32 such as anomalous pulmonary veins, vascular ring, pulmonary sling, aorto-pulmonary collaterals, and aortic arch anomalies. In addition, patients with multiple visceral anomalies such as in heterotaxy syndrome33 (also known as isomerism)34 frequently need extracardiac assessment.

Echocardiography remains the main diagnostic tool in the neonates for cardiovascular imaging. However, there are certain instances where additional information needs to be obtained to confirm the diagnosis or add information when echocardiography has not been able to provide complete information. Historically, cardiac catheterization, which is an invasive procedure and needs general anesthesia, was performed to sort out some of the complex anatomy when echocardiography could not provide all the answers. With advancement in CT and MRI technologies, the need for cardiac catheterization as a diagnostic modality has largely become obsolete. Advancements in non-invasive complementary tools such as cardiac MRI and CT are extremely helpful as additional imaging modalities for obtaining high-quality imaging.

The tenets of full basic understanding of the cardiac anatomy should include imaging that sorts out abdominal situs, atrial situs, ventricular looping, great artery relationship, systemic and pulmonary veins, atrial and ventricular septal morphology, atrioventricular valves, semilunar valves, coronary arteries, great arteries, intracardiac and extracardiac vascular anomalies. The diagnostic utility of echocardiogram can be limited by poor acoustic windows.35

CARDIAC MRI IN THE NEONATES

Multimodality assessment of CHD is essential for anatomical and functional evaluation for diagnosis and planning.36 Indications for cardiac MRI in the neonate can be broadly classified into two categories:

  1. Based on cardiac MRI sequences

    1. Anatomy delineation

    2. Flow quantification

    3. Magnetic resonance angiography (MRA)

    4. Tissue characterization

  2. Based on clinical indications for a cardiac MRI study

    1. Complementary modality to avoid multiple echocardiographic scans when there are poor acoustic windows

    2. Understanding complex spatial orientation of the cardiac chambers

    3. Obtaining accurate volumes and function, including end-diastolic volumes and ejection fraction quantification, calculating Qp:Qs, regurgitation fractions of valves

      Example: Volumetric data to determine single ventricle vs biventricular repairs

    4. Sorting out coronary artery anatomy in select cases

    5. Tissue characterization to sort out cardiac masses and tumors

  3. To delineate extracardiac vascular anatomy accurately where echocardiogram is unable to sort out intricate anatomy of the aortic arch, pulmonary arteries, systemic veins, and pulmonary veins. Examples include:

    1. Branching pattern of the aorta, which may constitute a vascular ring

    2. Delineation of collateral vessels supplying pulmonary arteries from the aorta

    3. Pulmonary artery slings

    4. Aortic arch morphology for surgical planning, including cases of complicated coarctation of aorta and hypoplastic aortic arches

    5. Interrupted aortic arches with complicated branching patterns

    6. In cases like pulmonary atresia where one needs to sort out all the sources of pulmonary blood flow

  4. To assess airway issues secondary to vascular malformation or chamber enlargement causing compression. Examples include:

    1. Understanding tracheal anatomy in case of heterotaxy syndrome, or major lung abnormalities

    2. Tracheal anatomy to quantify the degree of stenosis secondary to vascular ring

  5. Postoperative period with patient instability to assess patency of aortopulmonary shunt, RV to PA conduit, any sources of external compression to the bronchus or the vessels, ventricular aneurysms, right ventricular outflow tract aneurysms after Norwood type I procedure with a Sano shunt, etc.

  6. Venous anatomy and abnormalities:

    1. Assess venous anatomy to make sure there is no superior vena cava (SVC) obstruction in patients with Glenn and after arterial switch operation

    2. Pulmonary vein abnormalities, which can include various forms of total anomalous pulmonary venous return, especially the mixed type, partial anomalous pulmonary venous return, and scimitar syndrome

  7. Obtaining 3D data sets for 3D printing and virtual reality

CARDIAC MRI TECHNIQUES

Performing a cardiac MRI is slightly tedious due to the fact that during the imaging period, there is dynamic motion of the heart coupled with respiratory motion, both of which interferes in image acquisition. Methods have to be taken to mitigate this with specialized sequences and breath-holding techniques, which could be voluntary or via sedation/general anesthesia. Sedation in neonates and young infants (<6 months old) can be achieved by scanning during their natural sleep after a feeding.37 It is beyond the scope of this article to go over the physics of different sequences utilized in cardiac MRI. We will briefly go over some of the common sequences used in routine clinical practice.

  1. Spin Echo Black Blood Imaging: These images are generally T1-weighted images with short echo times. The most common variants of this technique are fast (turbo) spin echo and single-shot fast (turbo) spin echo. They have high tissue to blood contrast with blood pool appearing black and the tissue appearing gray to white. This sequence is particularly useful to evaluate anatomy and relationships of blood vessels and airways. These are static images (Fig. 1A). This sequence is also forgiving when there are metallic artifacts when compared to steady-state free precision (SSFP).38

  2. Balanced Steady-state Free Precision (bSSFP): This is the work horse sequence of cardiac MRI where the blood pool is white and the tissue is black. The images obtained here are cine images and are in real time (Fig. 1B). This helps in assessing ventricular function, ejection fraction, valvular stenosis, and regurgitation. When there are artifacts and turbulent flow, conventional gradient recalled echo (GRE) cine sequences can be used.

  3. Phase-encoded Flow Imaging: This sequence is used to calculate flow measurements across the blood vessels (arteries, veins, and across the valves). This helps in calculating flow volumes, differential flow to each lung, pulmonary to systemic blood flow ratio (Qp:Qs), regurgitation fraction and peak gradients across the valves, collateral flow.

  4. 3D Gadolinium-enhanced Magnetic Resonance Angiography (3D-MRA): This sequence needs intravenous administration of a gadolinium-based contrast agent. Images are simultaneously acquired in three planes and hence are very helpful to perform 3-D volume rendering and multiplanar reconstructions (Fig. 1C). It is extremely helpful in defining vascular anatomy and to measure accurate lengths with orthogonal measurements.

  5. First-pass Perfusion Imaging: This is a not so commonly used in the neonatal population. It is obtained after the administration of gadolinium and helps is identifying perfusion defects signifying infarction or fibrosis.

  6. Late Gadolinium Enhancement Imaging (LGE): Generally obtained 10 minutes after the administration of gadolinium, this sequence is useful in identifying edema, scarring, and fibrosis. The areas of scar and fibrosis have greater distribution of volume of contrast, and hence, there is delayed washout of the contrast. This makes the areas appear bright as compared to the normal myocardium (Fig. 1D).39

  7. T1 and T2 Mapping: It can provide data on tissue characterization like assessing presence of scarring/fibrosis and edema without administration of the contrast agent. In addition, it can provide extracellular volume (ECV) calculation if we obtain postcontrast T1 images (Figs 1E and F).

Figs 1A to F: Representative images obtained by various sequences. (A) Image obtained with spin echo black blood imaging sequence where the blood pool is black; (B) Image obtained with balanced steady-state free precession (bSSFP) sequence where the blood pool is bright; (C) Volume-rendered image of aorta obtained with 3D-MRA; (D) Late Gadolinium enhancement image showing abnormal myocardium with arrow; (E) T1 parametric imaging in the short axis; (F) T2 parametric imaging in the short axis

CARDIAC CT IN THE NEONATE

Cardiac CT is a complementary modality to echocardiography or cardiac MRI used in the evaluation of CHD in the neonates. It provides a fast approach to high-resolution images for defining the cardiac anatomy. Current CT scanners provide a spatial resolution of 0.24 mm and temporal resolution as low as 66 ms, for better visualization of complex congenital cardiac anatomy. They also have a high pitch rate with multidetector technology that can acquire full anatomic coverage of the heart and chest within 0.25 seconds freezing most of the cardiac and respiratory motion. This alleviates the need for sedation or cardiac anesthesia in most cases. The advancement of technology of current CT scanners with the short scan times also greatly reduces the radiation dose.

Radiation Exposure

The goal of every cardiac CT scan is to achieve the highest resolution images ensuring a radiation dose of as low as reasonably achievable (ALARA). However, cumulative radiation dose can be high particularly in patients with complex CHD, based on the different tests that are undertaken in neonates that include chest X-rays, cardiac catheterization, cardiac CT and lung perfusion scans. This necessitates the need for inclusion of the most recent technology to minimize total radiation dose by prospective ECG-gated scans, modulation of tube voltage based on patient’s size, high-pitched helical scanning, and iterative reconstruction techniques.40,41 With today’s third-generation multidetector-row computed tomography (MDCT) scanners, the radiation dose can be very minimal. We try to achieve submillisievert (less than 1 mSv) radiation dose exposure for most studies with excellent definition of their cardiac anatomy.42 Most neonatal scans are limited to a dose of 70kVp and field of coverage is minimized based on the structure being imaged.

CT Angiogram Imaging Modalities

  1. Dual-source helical computed tomography scanner with ultra-fast, low dose, high-pitch scanners referred to as FLASH imaging (Siemens Healthcare, Forchheim, Germany). New scanners include the technology of dual-source computed tomography with prospectively ECG-triggered data acquisition by maintaining high pitch values. This helps minimize the total radiation dose by very short scan times with an approximate imaging window of 250 ms. Recent scanners with high pitch values of up to 3.4 when used can cover the entire volume of heart in one single cardiac cycle with high-resolution image quality and radiation doses in the submillisievert range.43,44

  2. Retrospective EKG-gated imaging: Prospective and retrospective gated cardiac imaging performed to minimize artifacts caused by cardiac motion. Prospective gated imaging performs well when acquired with heart rates less than 90 bpm and may be a limitation in the neonate. When detailed coronary anatomy or cardiac volumes need to be acquired, the usual technique is retrospective EKG-gated cardiac imaging. This involves acquiring images through various phases of the cardiac cycle. This uses a lower pitch with resultant increase in the radiation dose.45

Preparation of the Neonate for a CT Scan

Prior to any CT scan, it requires that the primary and cardiac teams review the necessity of advanced cardiac imaging and the direct outcomes for patient management weighing the risk of radiation exposure. Next would be to review renal function and allergies. If a neonate has abnormal renal function, other modalities of imaging should be explored or imaging delayed until the recovery of renal function. The next important step is evaluating the need for sedation. Most neonates can be calmed adequately using sucrose solution with a pacifier prior to the scan.46 Motion can be minimized by feeding the baby prior to scan and comfortably swaddled in a blanket. However, for coronary artery delineation, the patient may need sedation with or without intubation, especially when breath holding is required to minimize motion artifacts, as in the case of a patient with d-transposition of the great arteries (TGA). A reliable peripheral intravenous catheter (PIVC) is required for contrast delivery. It can be of either a 24-G or a 22-G catheter. An umbilical venous or arterial catheter or a regular peripherally inserted central catheter (PICC) in general cannot be used for contrast delivery as they are not rated for power injections. This poses the risk of catheter tear and embolization during power injections. Routinely contrast in neonates is injected using a power injector with a pressure rating of 100–150 psi.

Contrast

For cardiac CT imaging, non-ionic iodinated contrast (iohexol, iopamidol, iopromide) is the standard of care. Dosing is usually limited to 2 mL/kg. Pediatric allergic reactions are rare, and management is similar to other allergic reactions with antihistamines, steroids, epinephrine, and bronchodilators.

Indications

The current indications for cardiac CT in neonates are listed below in order of what is more commonly used. Most of the acquisitions can be obtained by using a FLASH technique as described earlier (Fig. 2) and by retrospective gating for coronary imaging (Fig. 3).

Figs 2A and B: CT Flash images from a neonate at day of life 3 with d-transposition of the great arteries. Imaging performed to delineate the great vessel and aortic arch anatomy. Transverse aortic arch (TAo) was hypoplastic (A) Anterior view; (B) Posterior view. (LV, left ventricle; RV, right ventricle; RA, right atrium; LA, left atrium; AO, aorta; PA, Pulmonary artery; RPA, right pulmonary artery; LPA, left pulmonary artery; TAo, transverse aortic arch; DAo, descending aorta)

Fig. 3: Retrospective gated CTA in a neonate with d-transposition of the great arteries showing a single coronary artery that arises from the left anterior facing sinus of the aorta and divides into the right coronary artery (1), the left main coronary artery (2) and a prominent conal branch (3). (LV, left ventricle; RV, right ventricle; AO, aorta; MPA, main pulmonary artery). (A) It shows 3D reconstruction from the acquired imaging data; (B) MIP images of aorta with coronary arteries

Aortic Arch Anatomy

Various aortic arch anomalies can be present at birth (interrupted aortic arch, double aortic arch, vascular rings, supravalvar aortic stenosis) or develop within the first few days (coarctation of aorta). Diagnosis and delineation of aortic arch anomalies can be easily obtained by an ECG-gated or non-gated flash CT imaging of the chest. Usually, no sedation is required, and the patient can be fed and swaddled. Image acquisition is performed based on contrast opacification of left ventricle or aorta.

Pulmonary Artery Anomalies

Pulmonary artery anomalies are imaged with a similar technique as aorta. However, image acquisition timing may differ based on pulmonary arterial supply. With normal pulmonary arterial connections from the right ventricle outflow tract, image acquisition is timed based on opacification of the right ventricle. In patients with tricuspid or pulmonary atresia, usually pulmonary arteries are supplied by the patent ductus arteriosus, and timing of image acquisition is based on opacification of aorta.

Abnormalities of Great Vessels

Congenital heart defects like d-TGA (Fig. 2), congenitally corrected TGA, and tetralogy of Fallot (TOF) usually require advanced imaging in neonatal life if early surgical intervention is required. This may be to delineate the size of the pulmonary artery and aorta, coronary artery anatomy, or the location of the ventricular septal defect. Usually, most of this can be accomplished by FLASH CT technique; however, if detailed coronary anatomy is required, it may necessitate retrospective ECG-gated coronary imaging. The scans are usually timed based on aorta opacification. Care should be taken to account for the anatomy and the presence of a ventricular septal defect. In TGA, based on the level of mixing between the right and the left side, the timing of contrast in the aorta could be quite variable. In neonates, this can be challenging given the small volume of contrast that can be used based on the body weight.

Congenital Coronary Artery Anomalies

Congenital coronary artery anomalies may exist in isolation or with other CHDs. Coronary arteries are quite small in infants with size ranging between 1 and 2 mm.47 This combined with high heart rates and respiratory motion makes coronary imaging challenging. Imaging coronary origins in infants can mostly be achieved without sedation and FLASH CT technique. However, in cardiac lesions like TOF or TGA, clear delineation of coronary course is important prior to surgical repair. In these cases, patients may need sedation with intubation to perform breath holds and minimize respiratory motion. Some centers have also included the use of beta-blockers routinely to decrease heart rates prior to coronary scans.48

Evaluation of Pulmonary Veins

Evaluation of pulmonary venous anomalies will depend upon the suspected defect. Total anomalous pulmonary venous return (TAPVR) can be supracardiac, cardiac, intracardiac, or mixed type. Usually, the scan timing can be based on left atrial opacification. This scan range will depend upon the suspected drainage of the pulmonary veins. If infracardiac pulmonary venous drainage is suspected, the scan range should include subdiaphragmatic region up to the renal arteries. If anomalous venous drainage is suspected into the SVC draining to the right side, clear delineation of the anatomy may be accomplished by obtaining a peripheral intravenous route in the lower extremity for contrast administration.

Evaluation of Systemic Venous Anomalies

If systemic venous anomaly like interrupted inferior vena cava with azygous continuation or persistent left SVC is suspected, it may be required to image the systemic veins. This is usually accomplished by a delayed scan after contrast injection. The delay to image the venous recirculation can be based on the heart rate and presence of any intracardiac shunting. This generally can be accomplished by scanning between 30 and 45 seconds after contrast injection. If an arterial scan is required prior to the venous phase, it can be obtained with opacification of the aorta followed by a delayed scan 30–45 seconds later.

Evaluation of Single Ventricle Anatomy and Estimation of Ventricular Volume

Patients born with hypoplastic left or right ventricle, or an unfavorable anatomy that results in eventual single ventricle palliation, may need surgical intervention in the neonatal period. The usual CHD that undergo a single ventricle palliation include hypoplastic left heart syndrome, tricuspid atresia, pulmonary atresia with hypoplastic RV, unbalanced atrioventricular canal defect, and double inlet left ventricle. These patients may require delineation of their arterial anatomy and occasionally evaluation of their ventricular size prior to stage I palliation. The initial palliation in these cases may include a Blalock-Thomas-Taussig shunt, Sano shunt, or occasionally a hybrid procedure, which involves stenting of the patent ductus arteriosus and placement of branch pulmonary artery bands to limit the pulmonary blood flow. CT imaging for these patients can be accomplished usually by FLASH CT. Occasionally when coronary artery anatomy or ventricular volumes are required, a retrospective gated cardiac scan may be necessitated.

Image Analysis, 3D Image Reconstruction, and Printing

Many advanced software applications are available to further process the data sets obtained by cardiac MRI or cardiac CT. Cardiac MRI data can be post-processed to obtain three-dimensional images of aortic arch, pulmonary arteries, pulmonary veins, and coronary arteries. Further, the endocardial and epicardial borders can be traced out to determine ventricular volumes and function. MRI provides a reference standard for the evaluation of cardiac function.49

Cardiac CT images can be further evaluated by processing to create high-resolution 3D images. Multiplanar reconstruction (MPR) images can be used to present structural anatomy and accurate measurements by orthogonal measurements by double oblique technique. Processing software can also determine vessel diameter in the areas of narrowing or stenosis. When imaged through the cardiac cycle, cine images can be created to demonstrate the changes in intracardiac structure and anatomy or extracardiac vessel diameters during the cardiac cycle.

From the acquired cardiac CT or cardiac MRI images, three-dimensional printing of the cardiac and extracardiac structures can be accomplished to further aid the understanding of the anatomy and surgical planning.50 This is especially applicable in patients with double outlet right ventricle, aortic arch malformations, and patients with complex TOF, especially the cases with major aorto-pulmonary collaterals (MAPCAs).51

CONCLUSION

Neonatal cardiac imaging is a complex and exciting field that provides rapid and accurate diagnosis of neonatal anatomy and physiology to determine the optimal management. Fetal echocardiography and transthoracic echocardiography provide the initial tools in delineating the complex anatomy. For successful medical management and surgical intervention, some of these cardiac lesions require advanced cardiac imaging by cardiac MRI or CT. Indications for cardiac CT or cardiac MRI should be determined based on the requirement of anatomical or functional details in the presenting cardiac defect. With recent advances in both fields, this can be accomplished with minimal adverse effects. With the introduction of faster and efficient cardiac CT scans, the radiation dose is minimized. In the field of cardiac MRI, the use of specific neonatal magnetic coils and 3T scanners will help in getting images of better resolution in a shorter period. Ongoing research and advances in both fields with the complementary role of 3D models and virtual reality imaging project a more dynamic and exciting future in the field of neonatal cardiac imaging.

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