Magnetic Resonance Imaging in Pediatrics

Magnetic Resonance Imaging in Pediatrics

Symposium on Pediatric Radiology Magnetic Resonance Imaging in Pediatrics Madan v. Kulkarni, M.D.,* Sandra G. Kirchner, M.D.,t Ronald R. Price, Ph.D...

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Symposium

on Pediatric Radiology

Magnetic Resonance Imaging in Pediatrics Madan v. Kulkarni, M.D.,* Sandra G. Kirchner, M.D.,t Ronald R. Price, Ph.D.,t Danny Eisenberg, M.D.,§ and Richard M. Heller, M.D·II

Magnetic resonance (MR) imaging is a new diagnostic imaging technique that should be especially attractive to pediatric practice, since it does not utilize ionizing radiation, and, to this date, has not been shown to produce any significant biologic effect. Although this .imaging modality is in its early stages of development, clinical experience has suggested that MR combines the advantage of anatomic imaging with excellent soft tissue contrast and tissue characterization. This technique also offers the potential for revealing biophysical information unavailable at this time by any other modality. This report explains the basic prinCIples of MR imaging and also discusses the current practices in clinical MR imaging in children. The appropriate indications for MR imaging and future developments, such as MR spectroscopy, surface coil techniques, and the use of paramagnetic contrast agents are mentioned.

BASIC MAGNETIC RESONANCE PRINCIPLES Magnetic resonance utilizes the inherent magnetic properties of the nuclei of atoms such as hydrogen 1, sodium 23, fluorine 19, and phosphorus 31, each of which have odd numbers of protons and/or neutrons. Due to their pattern of nuclear content, these nuclei spin around a central axis and thus develop a magnetic field. The strength and orientation of this field is specified by its magnetic moment. When nuclei possessing these magnetic properties are placed in a strong external magnetic field, the net magnetic Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, Tennessee *Assistant Professor tProfessor ;j:Associate Professor §Clinical Fellow IIProfessor PediatriC Clinics of North AmeriCa-Vol. 32, No.6, December 1985

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Figure 1. This diagrammatic representation of the magnetic resonance signal demonstrates that nuclei in the natural environment are spinning along their individual axes with their individual magnetic moments distributed randomly (A). When these nuclei are placed in a strong magnetic field (Bo), they try to align themselves in a direction either parallel or 1800 opposed to the Bo field (B). Some of the individual magnetic moments will cancel each other's effect, but the net effect of the magnetic moment (m) will be parallel to the Bo field (B): By applying external radio frequency (RF), the net magnetic moment (C) can be tilted 900 to its original direction (D). Now the RF is discontinued and the magnetic moment will try to realign itself with the original Bo magnetic field. During this process of recovery, it gives off an RF signal, which is recorded as an MR signal (E).

moment (sum of the magnetic moment from the individual nuclei) will be oriented parallel to the axis of the external field. By applying an external radio frequency signal at a frequency unique to the nuclei under study, this net magnetic moment will begin to precess or rotate about the field direction and can be tilted 90 or 1800 from its original axis (Fig. 1). When the external radio frequency pulse is discontinued, the nuclei will return to their original orientation in the strong magnetic field. During this latter process they produce a radio frequency signal, which is recorded as the magnetic resonance signal. The magnetic resonance imaging system has the ability to record this signal, which originates from different points within a patient's body at a given level in X and Y coordinates. This signal intensity tnap in a given transverse sagittal or coronal plane will provide a tomographic image. The signal acquired in such a process is due to a combination of tissue-specific MR parameters such as the nuclear density, relaxation times, which are called T1 and T2, and blood flow. The soft: tissue contrast in an MR image can be altered by acquiring images that preferentially weight one of these parameters. Unlike computed tomography (CT), which depends on x-ray attenuation alone, the magnetic resonance imaging can be performed, manipulated, and altered using different pulse sequences to vary the relative contribution of nuclear density, T1, or T2. A basic imaging technique called the spin echo (SE) pulse sequence is demonstrated in Figure 2A; it utilizes a 900 pulse followed by a 1800 pulse. The result of this sequence is called an .. echo." The 1800 pulse is a phase-correcting pulse that brings the precessing

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nuclei into the same phase of rotation and provides the maximum available signal. If the time interval (TE) between the gO-degree pulse and the echo is varied, the resulting image will have a varying degree of T2 weighting. Since the MR signal is generally quite small, the entire pulse sequence may be repeated after a certain time interval (TR) and the resulting signals averaged to reduce noise. By keeping TE constant and increasing TR, the relative Tl contribution to the image can be altered. Another imaging. technique called an "inversion recovery pulse sequence" will also provide Tl-weighted images (Fig. 2B). The T2-weighted images have been found to provide the best soft tissue contrast between normal and abnormal tissue. Recent developments in software have provided an ability to acquire multiple pulse sequences (multiecho) in a multislice format in a single acquisition, and, as a result, have dramatically decreased the average time required to perform a patient study. Spin echo techniques with short TE (i. e., 30 msec) and TR (i. e., 500 msec) provide images that primarily document tissue contrast as a reflection of Tl relaxation times. These images (SE 30/500), along with inversion recovery (IR) images, demonstrate areas of long Tl relaxation times (long with respect to TR) as areas of decreased signal intensity (black)-for example, cerebrospinal fluid (CSF). On the other hand, tissues such as fat, a) Spin Echo Sequence ~----------------------TR----------------------~'I

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Figure 2. The spin echo (SE) pulse sequence (Fig. 2A) has a 90° pulse that is followed by a 1800 pulse after a time interval (T). The echo pulse is generated after another time interval (T). The time between the 900 pulse and echo pulse is called echo delay time (TE). The entire sequence is repeated after a time interval called pulse repetition rate (TR). By increasing the TE interval, relative T2 information in the image can be increased. In the inversion recovery (IR) pulse sequence (Fig. 2B) a 1800 pulse is followed by a spin echo sequence after a time interval called the inversion time (TI). The entire pulse sequence is repeated after a time interval TR. The IR sequence provides relatively Tl-weighted images.

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which have relatively short Tl relaxation times, give high signal intensity (white)-for example, subcutaneous fat and bone marrow. The SE images with long TE are relatively T2-weighted (SE 120/2000), and tissues with long T2 relaxation times (CSF) provide bright signal, while tissues with relatively shorter T2 relaxation times (white matter) have decreased signal intensity. TECHNIQUES FOR MAGNETIC RESONANCE IMAGING IN PEDIATRIC PATIENTS Prolonged scanning times for MR imaging require a quiet, cooperative patient, and a protocol for sedation similar to that fOJ:" computed tomography can be used. Since the strong magnetic field interferes with ferromagnetic devices, equipment for general anesthesia cannot be used in the MR room at this stage of development. Patients with intracranial ferromagnetic surgical clips or with recently placed vascular clips are not studied because the strong magnetic fields might displace these materials. Patients with cardiac pacemakers are also not examined, since the radio frequency used in MR imaging might interfere with the cardiac pacemaker mechanism. 13 Due to local field distortion, ferromagnetic dental fillings as well as surgical clips and staples can cquse artifacts in MR imaging. Physiologic motion, such as respiration, cardiac contraction, and peristaltic waves also cause image degradation. CLINICAL UTILIZATION It has been noted that abnormal tissues have different Tl and T2 relaxation times as compared with normal tissues, and MR imaging uses this principle to detect pathology. The plane of imaging and selection of pulse sequences is predetermined by the organ examined. For example, sagittal images are preferred in the spine, and coronal planes are selected for examination of the hips. After the initial scans are completed, additional itp.ages can be obtained in different planes' as well as varying pulse sequences according to the detected abnormality. Cardiac and respiratory gating can also be used to reduce motion artifact. In imaging pelvic organs, distension of the urinary bladder helps to displace bowel loops out of the pelvis.

THE CENTRAL NERVOUS SYSTEM

Initially, . MR imaging was employed only in intracranial and spinal cord diseases because the brain and spinal cord are not significantly affected by respiratory or cardiac motion. As compared with x-ray CT, MR has improved the lesion detectability in posterior fossa and brain stem disease. Intracranial neoplasms are seen in MR imaging owing to the different Tl and T2 relaxation times in tumors as compared with the normq} gray and white matter. Similarly, edema surrounding the neoplasm is readily

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detected, since changes in tissue water content affect the relaxation times. The proper use of pulse sequences will enhance the differences between the Tl and T2 relaxation times in tumor as compared with normal brain. By changing the gradient angles, sagittal, coronal, and nonorthogonal images can be performed (Fig. 3). The magnetic reso~\ ance imaging not only has shown improved sensitivity in tumor detection b has also improved image localization with use of multiplanar MR imaging. T e increased Tl and T2 relaxation times seen in malignant brain tumors are not specific, and they are seen in benign lesions as well. Posterior fossa tumors along with associated changes of obstructive hydrocephalus are well recognized by MR. The ability of spin echo images to detect edema at the ventricular margins has been demonstrated, and diminishing periventricular edema after shunting has been documented on MR images. 8 A significant limitation of MR is its inability to identifY calcification within neoplasms. 22, 24 This is a major disadvantage, since characterization of a mass on the basis of the presence of calcification, which is easily done with the use of x-ray CT, is not possible with magnetic resonance imaging. Another limitation is the inability of current MR systems to differentiate tumor and edema on the basis of their relaxation times. Future development in paramagnetic contrast agents may be helpful in the discrimination of intracranial lesion and associated edema. 16 The excellent contrast demonstrated between gray and white matter in MR imaging is due to the difference in their Tl relaxation times. IS Since these relaxation times are dependent on the stage of myelinization, MR is useful in demonstrating myelinization disorders in children. 8 In demyelinating diseases, multiple focal areas of increased signal intensity are seen

Figure 3. A, Sagittal spin echo (SE) image with TE of 30 msec and TR of 1000 msec (SE 30/1000) in a patient diagnosed initially to have a corpus callosum glioma by an x-ray CT scan. On this MR image the glioma (open arrow) is clearly seen inferior to the corpus callosum (curved arrow) and separate from it. The tumor has areas of varying signal intensity related to necrosis as well as hemorrhage. B, Coronal SE 30/1000 image also demonstrated the glioma arising from and obliterating the region of the third ventricle. The lateral ventricles (arrowheads) are displaced and compressed by the tumor (black arrow).

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Figure 4. Postinfective demyelinating disease on SE 60/2000 pulse sequence demonstrates multiple areas of increased signal intensity in white matter (arrowheads). The T2-weighted pulse sequence (TE = 60 msec) shows prolonged T2 relaxation times within the lesions.

in the periventricular white matter on T2-weighted pulse sequences. However, these findings are nonspecific and are seen in a variety of demyelinating processes. Although separation of gray and white matter is superior on inversion recovery pulse sequences, the T2-weighted spin echo sequences demonstrate these demyelinating processes more effectively. These T2-weighted sequences are in turn more sensitive than x-ray CT. 23 Our early experience with pediatric demyelinating diseases (Fig. 4) tends to confirm that sensitivity. Sagittal MR images of the brain stem and cervical cord have improved the detection and understanding of disease processes such as syringomyelia, intra-axial tumors, spinal stenosis, and Arnold-Chiari malformations. 7. 21 The sagittal images can clearly show herniation of the cerebellum inferiorly through the foramen magnum into the cervical region. Syringomyelia (Fig. 5) and syringobulbia are also accurately identified with MR imaging, not only because of demonstration of enlargement of the cord but also because of the cavitation within the spinal cord or the brain stem. Tumors in the region of the spinal cord or the brain stem are often well seen with MR, and tend to produce enlargement of the spinal cord. Figure 6 illustrates a sagittal image of a patient with astrocytoma of the brain stem with an abrupt change between the size of the normal and abnormal brain stem. Although sagittal MR is generally used in the detection of spinal pathology, the transverse images are helpful in the diagnosis of diastematomyelia (Fig. 7). On the other hand, coronal images can also be used in determining extent of pathologic processes such as arterial venous malformation of the spinal cord. 9 Since CSF acts as an intrinsic contrast material, the insertion of an intrathecal contrast agent is not necessary.

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THE CHEST AND MEDIASTINUM

The inherent soft tissue contrast resolution of MR imaging has been shown to be very useful in thoracic imaging. 1 Since blood flowing in vascular structures does not provide a detectable MR signal, the vessels are naturally well contrasted with mediastinal structures, and the use of intravenous contrast is not necessary. On the other hand, fat within the mediastinum shows a bright signal due to its short Tl relaxation time, and fat can be distinguished from tumors within the mediastinum on the basis of differences in their Tl values. 6 Thus, children with a mediastinal mass are effectively examined with MR imaging. For example, the abnormal lymphadenopathy in lymphoma has decreased signal intensity as compared with the normal mediastinal fat and is contrasted extremely well with the normal blood vessels (Fig. 8). In a recent study, MR detected additional diseases in 25 per cent of the cases with mediastinal lymphadenopathy as compared with x-ray CT.3 Vascular obstruction caused by mediastinal masses can also be documented with MR. 19 Lymphadenopathy in the cervical region is also detected with MR, since these lymph nodes have a different Tl relaxation time as compared with normal muscle. Normal thyroid tissue as well as thyroid masses can be detected by MR in transverse and coronal planes, and the presence of thyroid tissue in the mediastinum can be documented. 17

THE HEART

Cardiac imaging with MR, although in its early stage of development, shows promise for providing multiplane cardiac images with R-wave gating.

Figure 5. A, A cervical syringomyelia is shown as decreased signal intensity in the enlarged cervical cord (arrowheads). The syrinx cavity on this Tl-weighted sagittal MR image has signal intensity similar to CSF surrounding the cord. Normal size cervical cord (white arrow). B, Inversion recovery pulse sequence at the same level demonstrates decreased signal intensity (arrowhead) in the syrinx cavity and CSF surrounding the cord (white arrow) owing to their prolonged Tl relaxation times. Cerebellum (C) and pons (P) are also well seen .

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Figure 6. A, Sagittal MR image with SE 30/315 technique demonstrates enlargement of the pons and brain stem. An area of decreased signal intensity posteriorly (arrow) has signal intensity similar to CSF (curved arrow). B, On a T2-weighted pulse sequence (SE 150/2000) abnormal signal intensity is noted within the tumor, and previously described area now has a bright signal (arrow) similar to CSF (curved arrow). This area probably represents a cystic component within the tumor, which was diagnosed as a cystic astrocytoma. C, A SE 30/200 image performed after radiation therapy demonstrates a decrease in size of the neoplasm and resolution of the cystic component.

Figure 7. Diastematomyelia in the thoracolumbar region is demonstrated in this transverse SE 30/500 image. Two cords (arrowheads) are seen within the spinal canal. Vertebrae (V) and kidneys (K) are also noted.

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Figure 8. Mediastinal lymphadenopathy in Hodgkin's lymphoma (arrowheads) has intermediate signal intensity as compared with muscle (M) and fat (black arrow) on SE 30/500 pulse sequence. Aortic arch (A). Right and left brachiocephalic veins (white curved arrows) and trachea (white straight arrow) are also documented.

The absence of signal from flowing blood allows for excellent contrast between blood and the myocardium and, thus, also provides for good depiction of chamber anatomy. Abnormal chamber enlargement, myocardial hypertrophy or thinning, congenital defects such as atrial or ventricular septal defects, and abnormal vascular connections can be documented. Patients with congenital heart lesions can also be studied with MR after corrective surgery. Vascular patency and intracardiac chamber relationships can be documented without using intravenous contrast agents (Fig. 9). The normal pericardium, which is 2 to 3 mm thick, does not show appreciable signal on MR imaging. An abnormally thick pericardium is suspicious for either pericardial effusion, fibrosis, or infection, and varying pulse sequences can be used to differentiate pericardial thickening from effusions. 19 Pericardial cysts can be diagnosed with MR and the content of the pericardial cyst can be further characterized using Tl- and T2-weighted images. Intracardiac thrombus or masses can also be demonstrated with MR, since these lesions produce abnormal signal within the chamber cavity.

Figure 9. A, Cardiac gated coronal SE 30/500 image in a patient with transposition of the great vessels post-Mustard procedure shows that the superior vena cava (arrow) is diverted medially toward a pericardial bafRe. B, The inferior vena cava (arrow) opens into the left atrium by a pericardial bafRe and the right upper lobe pulmonary vein (arrowheads) opens into the right atrium (RA). The smooth, thick-walled left ventricle (LV) communicates with the pulmonary artery (PA). Right pulmonary artery (RPA) .

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Figure 10. A, A large Wilms' tumor (T) on SE 30/500 sequence has decreased signal intensity as compared with the liver (L), which is displaced anteriorly and toward the left by the tumor. The hepatic vasculature (arrowhead) is seen as areas of markedly decreased signal intensity due to Howing blood. B, Coronal SE 30/500 image demonstrates the inferior vena cava to be displaced and compressed (arrowheads) by the Wilms' tumor (T). (From Kulkarni, M. V., et aI.: J. Nuc!. Med., August, 1985.) THE ABDOMEN

Magnetic resonance imaging of the abdomen and pelvis has thus far shown encouraging results. However, due to the prolonged imaging times involved in MR, respiratory motion causes significant artifact. The use of respiratory gating can greatly improve image quality.15 As with x-ray CT, the lack of intra-abdominal fat in infants and young children causes poor definition of the intra-abdominal and pelvic tissue planes. Although the spatial resolution of MR is slightly inferior to that of x-ray CT, the soft tissue contrast is excellent. The visualization of retroperitoneal and hepatic vasculature is also excellent with MR. Intrahepatic lesions can be diagnosed with MR because of their abnormal Tl and T2 relaxation times. Renal masses are detected in the same manner and can be examined in multiple planes. The vascular invasion or compression by a renal tumor can be evaluated without the use of intravascular contrast agents (Fig. 10). Renal cysts can be differentiated from renal tumors on the basis of their relaxation times. 10 Pancreatic imaging is possible with MR but requires use of oral contrast agents such as ferrous gluconate and respiratory gating. MR imaging should also prove to be useful in detecting enlarged lymph nodes in the peripancreatic area. The retroperitoneal nodes, in cases of lymphoma and renal and adrenal tumors, can be detected with or without respiratory gating (Fig. ll). The early data on pancreatic20 and other retroperitoneal diseases have shown encouraging results, although at present x-ray CT appears to be the superior imaging modality. Further developments in MR technology

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Figure 11. Metastatic retroperitoneal neuroblastoma on T2weighted image demonstrates abdominal aorta (arrowhead) displaced anteriorly by lymph node mass (M). Liver (L) has decreased signal intensity on this T2weighted image as compared with lymphadenopathy. Also, respiratory artifacts are seen as multiple parallel lines in this nongated image.

will improve its performance in the detection of abdominal disease processes. THE SKELETAL SYSTEM

The high signal intensity of fat within the normal bone marrow makes MR an excellent imaging modality for skeletal disorders. Although cortical bone has markedly diminished signal on MR, the technique has allowed for coronal and sagittal images that have significantly improved the detection and documentation of extent of skeletal abnormalities.

Figure 12. Coronal SE 30/500 image in Legg-Perthes' disease shows a normal femoral head on the right while marked disorganization of the proximal femoral epiphysis is seen on the left. Bladder (B).

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Figure 13. A, Osteomyelitis of the left tibia has abnormal bone marrow signal intensity (arrow). The cortical bone and edema surrounding the cortical bone cannot be differentiated on this SE 30/1000 pulse sequence. B, A T2-weighted image (SE 60/1000) obtained at the same level demonstrates increased signal from the edema (arrowheads), while cortical bone continues to show decreased signal intensity.

The diagnosis of avascular necrosis of the hips, including that due to Legg-Perthes' disease, is well suited to MR imaging (Fig. 12), which provides results superior to conventional radiography. The detection and extension of the bone tumors2 as well as marrow replacement by leukemic infiltrates 4 can be identified on MR imaging. MR has also demonstrated increased sensitivity in detecting osteomyelitis as compared with conventional radiography5 because of its ability to detect extraskeletal abnormalities and changes within the marrow (Fig. 13). CURRENT AND FUTURE DEVELOPMENTS Recent developments in MR surface coil techniques have provided the ability to image small and superficial structures such as the spine, orbits, knees, and thyroid gland. Marked improvement in the MR signal has also allowed magnification of images with improved spatial resolution. In addition, there is currently great interest in the development of paramagnetic contrast agents, which could dramatically improve diagnostic specificity. These agents have been used to differentiate intracranial lesions from edema in animal models, and early results from human subjects have demonstrated similar findings. Active research in proton spectroscopy as well as in vivo analysis of nuclei such as 13C, 19F, 23Na, and 31P is occurring and hopefully will provide noninvasive methods for spectroscopy using MR. In addition, the chemical shift analysis of phosphorus metabolites also shows great potential for improved tissue characterization.

SUMMARY Magnetic resonance imaging has potentially broad applications in pediatriC practice. Although further studies are needed to determine its exact role in comparison with the other imaging modalities, magnetic resonance has shown increased sensitivity in lesion detection in many disease processes. Since MR does not use ionizing radiation and does not

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require intravenous contrast to identify vascular structures, it becomes an ever more attactive imaging tool for pediatric diagnosis. Thus, the early results of MR imaging have shown promise and the future of MR appears exciting. ACKNOWLEDGMENTS The authors wish to thank the Department of Pediatrics and the Center for Medical Imaging Research at Vanderbilt for their cooperation and use of resources. We also wish to acknowledge Joann Fields and Carolyn Cooper for manuscript preparation, the technical advice from Drs. C. L. Partain, J. N. Lukens, A. C. Price, and A. E. James, and the editorial assistance of Mary Henry.

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20. Stark, D. D., Moss, A. A., Goldberg, H. I., et al.: Magnetic resonance and CT of the normal and diseased pancreas: A comparative study. Radiology, 150:153-162, 1984. 21. Yeats, A., Zawadski, M. B., Norman, D., et al.: Nuclear magnetic resonance imaging of syringomyelia. A.J.N.R., 4:234-237, 1983. 22. Zawadski, M. B., Bradami, J. P., and Mills, C. M.: Primary intracranial tumor imaging: A comparison of magnetic resonance and CT. Radiology, 150:435--440, 1984. 23. Zawadski, M. B., Davis, P. L., Crooks, L. E., et al.: NMR demonstration of cerebral abnormalities: Comparison with CT. A.J.R., 140:847-854, 1983. 24. Zimmerman, R. A., Bilaniuk, L. T., Goldburg, H. 1., et al.: Cerebral NMR imaging: Early results with a 0.12 tesla resistive system. A.J.R., 141:1187-1193, 1983. Department of Radiology and Radiological Sciences Vanderbilt University Medical Center Nashville, Tennessee 37232