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Pediatr Radiol (1989) 20:10-19

Pediatric

Radiology

9 Springer-Verlag 1989

Abdominal magnetic resonance imaging

T. M. Harris and M. D. Cohen

Riley Hospital for Children, Indiana University School of Medicine, Indianapolis, Indiana, USA

Abstract. A review of the first five years of experi- ence with pediatric abdominal Magnetic Resonance Imaging (MR) is presented. The abdomen is exam- ined organ by organ with description of normal anat- omy and pathological processes. Practical clinical uses of MR are indicated. There is a brief review of motion artifact supression techniques.

There has been nearly five years of experience with Magnetic Resonance Imaging (MRI) in the pediatric population. Comparison of MRI with other imaging modalities has been made in nearly all organ sys- tems. Advantages of MRI which have been pro- posed include lack of ionizing radiation, superior blood vessel visualization without intravenous con- trast, improved contrast resolution and multiplanar imaging. This review attempts to summarize the im- pact of MRI on abdominal imaging in pediatric pa- tients.

Liver

Vasculature and biliary tree

The normal hepatic vasculature is well seen on MR without the use of IV contrast. The transverse plane has been shown to be the most valuable for evalu- ation of the liver vasculature with greater than 90% visualization of the IVC; right, middle, and left he- patic veins; and fight and left portal w~ins [1]. In the pre-operative evaluation for liver transplantation, MR can be a useful complementary procedure to ultrasound in characterizing the portal vein [2]. The size, position, and patency of the portal vein can be successfully evaluated prior to transplantation. MRI can identify cavernomatous transformation of the portal vein as serpentine vascular structures in the porta hepatis [3]. Normal bile ducts are poorly visu- alized with MR but dilated ducts can be seen. Di- lated ducts are best seen with a combination of both T1 and T2 weighted SE sequences demonstrating de-

of both T1 and T2 weighted SE sequences demonstrating de- Fig. I a and b. Diagnosis:

Fig. I a and b. Diagnosis:Choledochal cyst. a Ultrasound in the sagittal plane demonstrates dilated common hepatic duct and common bile duct (arrows). Liver (L). b SE 30/500. A rounded area of low signal intensity consistent with bile (B) is seen below the portal vein (arrows) con- firming the presence of dilated extraheptic biliary tree. Aorta (A), Infi~rior Vena Cava

(I)

T_ M. Harris and M. D. Cohen: Abdominal MRI

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T_ M. Harris and M. D. Cohen: Abdominal MRI 11 Fig.2a-e. Diagnosis: Hepatoblasto- ma. a SE

Fig.2a-e. Diagnosis:Hepatoblasto- ma. a SE 30/900 and

b SE 20/1500 Axial and coronal im-

ages demonstrate a large homo- geneous mass (arrows) arising fi'om the inferior aspect of the liver with splaying of hepatic vessels (curved arrow) around the margin of the mass. Normal, displaced right kid- ney (K) was clearly identified in both planes excluding a renal origin of the mass. c SE 90/1500 T2 weighted image demonstrates patchy increased signal in the mass

Fig.3a and b. Diagnosis:Neuro- blastoma with liver metastases.

a and

a left adrenal mass (arrow) with

mixed signal intensity. The liver (L)

has abnormally increased signal with a diffusely nodular appearance

Fig.4a-c. Diagnosis:Neuroblasto- ma with extensive liver metastases in newborn patient, a CT scan with intravenous contrast demonstrates massive hepatomegaly (L) with slightly inhomogeneous texture but without demonstration of focal le- sions. In retrospect there is also a low density lesion without calcifica- tion in the right adrenal region (arrow). Stomach (S), Spleen (sp).

b SE 16/550 The liver (L) shows ab-

normally decreased signal com- pared to spleen (sp) on T1 weighted image indicating a diffuse process, e SE 80/2000 T2 weighted image shows markedly abnormal increased 1"2 signal from liver with stretching and distortion of vessels (low signal) much better appreci- ated than on CT. This finding ~s consistent with metastatic disease. Primary tumor was poorly seen with MR

b SE 60/2000 Images show

creased signal compared to surrounding liver on T1 weighted images and increased signal on T2 [4]. All dilated segments of the intra and extrahepatic bil- iary tree are well visualized. However, ultrasound and computed tomography remain the proven non-

invasive methods for evaluation of the biliary tree. A choledochal cyst has been identified with MR as a mass with characteristics similar to bile (Fig. 1) [5]. However US and nuclear medicine DISIDA studies are usually adequate for evaluation.

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T.M.Harris and M.D.Cohen: Abdominal MRI

12 T.M.Harris and M.D.Cohen: Abdominal MRI Fig.Sa-c. Diagnosis: Cavernous hemangioma, aStrongly T1 weighted image

Fig.Sa-c. Diagnosis: Cavernous hemangioma, aStrongly T1 weighted image demonstrates well marginated round homogene- ous areas (H) of low signal intensity in the right lobe of the liver (L). Stomach (S). bSE30/500 Less T~ weighting makes lesion/liver

contrast less, but abnormality is still clearly evident (arrow).

c SE 60/2000 T2 weighted image shows characteristic appearance

of cavernous hemartgioma with well defined margins and marked homogeneous increased signal intensity. Stomach 48),Spleen (sp)

intensity. Stomach 4 8 ) , S p l e e n (sp) FJg.6a-e. Diagnosia: Hemangioendothelioma,

FJg.6a-e. Diagnosia: Hemangioendothelioma, a CT with in- travenous contrast demonstrates large low density liver lesion (H) with enhancing periphery characteristic of this tumor. b SE 30/500 and c SE60/1000. A large liver mass is demon-

Tumors

Malignant and benign mass lesions of the pediatric liver have been evaluated. In general, tumors have demonstrated T-1 and 3"-2values longer than normal liver resulting in hypointense areas on T1 weighted images and hyperintense lesions on T-2. Lesions have been more conspicuous on T-2 weighted im- ages. Hepatoblastoma (Fig.2), hemangioendothelio- ma, cystic hamartoma, and numerous metastatic tu- mors (neuroblastoma (Fig.3), islet cell, Hodgkins lymphoma) have been imaged and have shown the above characteristics [6]. Recently at our institution MR was helpful in characterizing massive hepato- megally in a neonatal patient. CT showed diffuse liver enlargement. MR revealed a diffusely nodular liver with abnormally increased T2 signal consistent with metastatic disease (Fig.4). Cavernous heman- gioma, a common liver tumor, has a specific MR ap- pearance and can be distinguished from liver metas- tases even though both lesions have prolonged T1 and T2 relaxation times (Fig.5). On strongly T2 weighted images cavernous hemangiomas are ovoid

strated with a central area of decreased signal on T1 weighting which becomes hyperintense on longer TR image. Note the mark-

edly enlarged hepatic artery (arrows) sweeping around the lesion

- a characteristic of hemangioendothelioma in our experience

or spherical with hyperintense homogeneous signal opposed to metastatic lesions which typically have less well defined borders and are heterogeneous in signal. These features in conjunction with higher contrast/noise ratios in hemangiomas can result in differentiation of these tumors from metastases with a 90% accuracy [7]. Although calculated T1 and T2 values have been shown to be of little value in distin- guishing various liver tumors [8], certain characteris- tics may be of use in distinguishing between tumor types. Ferrucci has reported that 25% of metastatic deposits demonstrate a bright peripheral halo sur- rounding an isointense or low intensity nodule on T2 weighted images [9]. This finding was not observed in benign lesions. Histologically, focal nodular hyperplasia of the liver demonstrates a stellate scar and this feature has been seen with MR [10]. The fi- brous pseudocapsnle of hepatoma has a characteris- tic low intensity peripheral rim on "1"1weighted im- ages [11]. In our experience, the markedly enlarged hepatic artery seen feeding an hemangioendothelio- ma is a characteristic finding of this disease (Fig. 6). There has been interest in the ability of MR to de- tect liver metastases [12, 13]. Recent work using a

T. M. Harris and M. D. Cohen: Abdominal MRI

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T. M. Harris and M. D. Cohen: Abdominal MRI 13 Fig.7a und b. Diagnosis: Hemochromatosis. b

Fig.7a und b. Diagnosis:Hemochromatosis.

b SE 60/2000. Note the homogeneous abnormally decreased sig-

nal from liver (L) on T2 weighted image. Spleen (S)

a SE 30/500

and

0.6 T magnet has shown that T1 weighted spin-echo (SE) imaging (with extensive signal averaging to de- crease motion artifact) is superior to T2 weighted im- aging in detection of hepatic metastases. Further work at this field strength has determined that T1 weighted SE and inversion recovery (IR) sequences are superior to contrast enhanced computed tomog- raphy for overall detection of individual metastases. However, other workers have found that at a field strength of 1.5 T, there is better focal liver lesion de- tection with T2 and proton density weighted sequen- ces (with respiratory compensation) than with T1 weighted images (with signal averaging) [14].

Diffuse processes

Fatty infiltration of the liver has been investigated in adult patients by proton spectroscopic imaging with encouraging results. Using a modified SE technique, "opposed" images can be generated which will dif- ferentiate fatty infiltration (decreased signal) from normal liver [15, 16]. Transfusional hemosiderosis (Fig. 7) has been investigated in children using a SE technique. Liver and bone marrow demonstrate ab- normally decreased signal. This is thought to be due to deposition of paramagnetic hemosiderin in liver and bone marrow [17]. Estimates of iron content in liver can be made by MR but cannot yet compete with the precision of dual-energy CT [18].

Contrast agents

Intravenous MR contrast agents gadolinium-DTPA and ferrite particles have been studied in liver im- aging. Contrast agents are used in order to increase conspicuity of lesions and possibly decrease scan time. In general, agents decrease both T1 and T2 re- laxation times. Following intravenous administra- tion, gd-DTPA is initially distributed in the intravas-

cular compartment and then diffuses into the ex- travascular spaces in both normal and abnormal tis- sues. Rapid imaging after administration of contrast with short TE/TR sequences has been necessary in order to preserve contrast between normal liver and lesions. Otherwise, delayed diffusion of gd-DTPA into abnormal tissue results in loss of contrast be- tween liver and lesion [9]. Ferrite particles are a promising new agent for liver imaging [19]. The par- ticles are phagocytized by the reticuloendothelial system (RES) in liver, spleen and bone marrow. The presence of ferrite markedly decreases T2 relaxation times of these tissues resulting in decreased signal on T2 weighted images. Tissues not containing RES ele- ments, e.g. metastatic tumor nodules, are unaffected and continue to produce signal. In animal models, ferrite has been effective in increasing signal dif- ferences between normal liver and tumor [20]. At the present time liver MR appears to be most useful in answering questions concerning vascular anatomy and in tumor detection. Various character- istics of focal lesions can be useful in determining the exact pathology.

Kidneys and adrenalglands

There has been extensive evaluation of the kidneys with MR. Renal margins can clearly be seen and renal cortex and medulla differentiated. The ability of MR to image in multiple planes, particularly coro- nal, is useful in differentiating renal from extrarenal processes and demonstrating associated vasculature (Fig.S).

Congenital anomalies and hereditary disorders

MR is capable of demonstrating congenital renal anomalies, cystic diseases, and hydronephrosis. However little added information over ultrasound (US) or excretory urography (EU) has been found except in differentiating renal agenesis from abnor- mal location of the kidney in some cases [21]. MR of patients with polycystic disease has been able to demonstrate hemorrhage into cysts. T1 weighted im- ages show increased signal intensity compared to

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T.M. Harris and M. D. Cohen: Abdominal M RI

14 T.M. Harris and M. D. Cohen: Abdominal M RI Fig.8a-c. Diagnosis: Neuroblastoma in ten-year-old female.

Fig.8a-c. Diagnosis: Neuroblastoma in ten-year-old female. a CT with IV contrast demonstrates large complex mass (m) in left abdomen displacing left kidney (k) posteriorly, b SE 40/900 and

e SE 90/2000 show extra-renal origin of mass (arrows) with com- plex signal characteristics

of mass (arrows) with com- plex signal characteristics Fig.9a und b. Diagnosis: Bilateral adrenal hemorrhage in

Fig.9a und b. Diagnosis:Bilateral adrenal hemorrhage in neonate. a SE 32/500 and b SE 60/2000 Triangular areas of increased sig- nal are seen in both suprarenal locations on both T1 and T2 weighted images indicating sub- acute hemorrhage in both adrenal glands (arrowhe~ids). Kidneys (K). [Reproduced with permission of Dr. David Cory]

simple cysts [22]. Imaging of patients with sickle-cell nephropathy has demonstrated decreased cortical signal on T2 weighted images [23].

Renal transplants

Imaging of renal transplants has been undertaken [24]. A transplant suffering from acute rejection dem- onstrates a decrease in corticomedullary differentia- tion (CMD) and an overall decrease in signal inten- sity. Complete loss of CMD has been found in chronic rejection. Acute tubular necrosis shows no particular pattern varying from good to absent CMD. Lymphocoeles can be distinguished from he- matoma by differences in relaxation times although the utility of this finding is questionable because US is usually sufficient for examination of peri-trans- plant fluid collections.

Infection

Acute pyelonephritis in children has been evaluated with MR but results have been discouraging due to lack of specific added information [25].

General adrenal disorders

Both normal and abnormal adrenal gl[ands are well visualized with MR. Adrenal hemorrhage, adenoma, hyperplasia, metastases and myelolipomas have been imaged [26]. MR of bilateral adrenal hemor- rhage has shown areas of increased signal on T1 and T2 weighted images [27]. Imaging was performed five days after the onset of symptoms which allowed the formation of paramagnetic methemoglobin

(Fig.9).

Tumors

Perhaps MRI will find one of its greatest pediatric abdominal applications in evaluation of renal and surrounding masses. Diagnosis of Wilms tumor and neuroblastoma, the two most common extracranial solid malignant neoplasms in children, typically in- volves multiple imaging modalities. US is the usual screening study of an abdominal mass in a pediatric patient. It can distinguish renal from extrarenal masses and cystic from solid masses. Cystic masses

T. M. Harris and M. D. Cohen: Abdominal MRt

T. M. Harris and M. D. Cohen: Abdominal MRt Fig.10a and b. Diagnosis: Wilm's tumor of

Fig.10a and b. Diagnosis: Wilm's tumor of the left kidney.

a SE 32/550 Transverse image demonstrates normal right kidney

(K) and well-defined homogeneous mass (M) arising from left kidney. Note good visualization of normal aorta (small arrow) and

inferior vena cava (large arrow) without IV contrast.

b SE t20/2000 T2 weighted image demonstrates increased signal

of mass (M) as is typical of this tumor. Gallbladder (arrow)

of mass (M) as is typical of this tumor. Gallbladder (arrow) Fig.ll. Diagnosis:Neuroblastoma. SE 30/500. There

Fig.ll. Diagnosis:Neuroblastoma. SE 30/500. There is extension

of the tumor mass from a primary adrenal location with encase-

ment and displacement of the celiac axis and its branches. Note exceptional blood vessel delineation without the use of IV con- trast. Celiac axis (arrow), tumor mass (t), IVC (c), Spleen (s), Liver

03

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usually require no further evaluation unless they are renal in origin. Vascular invasion can also be evalu- ated by US. Computed tomography (CT) is felt to be a better imaging modality for solid lesions because it can evaluate the primary tumor for location, calcifi- cation, nodal or liver metastases, spread across the midline, paravertebral extension and vascular en- casement. Both Wilms tumor and neuroblastoma have been studied with MR [28-31]. Coronal MR has been found to be most helpful in evaluation renal versus extrarenal origin of the mass and extension into surrounding structures. MR can demonstrate all the features seen by CT except calcification. The in- ability of MR to identify calcium may well be over- come by its multiplanar capability with better ability to identify the origin of a tumor. Belt, et al., were able to identify the renal origin of all fourteen Wilms tu- mors that they studied with MR. The tumor demon- strated signal characteristics consistent with pro- longed T1 and T2 relaxation times (Fig.10). Most tumors were inhomogeneous with signal nonunifor- mity corresponding to areas of necrosis and hemor- rhage. MR was able to identify hepatic metastases, enlarged lymph nodes, renal vein/inferior vena cava invasion and blood vessel displacement. In seventeen cases of neuroblastoma, Dietrich et al. [31], were able to identify the site of origin in all. MR successfully identified vascular involvement, bone marrow and dural metastases, and intraspinal and mediastinal spread of tumor. In our experience, MR better defines vessel encasement by tumor (Fig.ll) than CT and may prove more accurate at showing spread into the spinal canal. So far, the major potential for MR in renal and surrounding masses is that it might replace the

Fig.12a-c. Diagnosis: Splenic abscess, aCT scan shows two areas of low attenuation within spleen (A). Stomach (S). b and e SE 30/500 TI weighted axial and coronal images show two sep- arate areas of decreased signal intensity in spleen (,4,) consistent with abnormal fluid collections. On T2 weighted images (not shown), the abnormal areas had increased signal compared to sur- rounding splenic parenchyma

On T2 weighted images (not shown), the abnormal areas had increased signal compared to sur- rounding

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16 Fig.13. Diagnosis: Post-op anal pullthrough with rectum (arrow- head) positioned outside of levator sling (arrow)

Fig.13. Diagnosis:Post-op anal pullthrough with rectum (arrow- head) positioned outside of levator sling (arrow)

use of multiple other modalities including CT, US and sulphur colloid scanning. Unfortunately, MR has yet to consistently provide new and unique in- formation, e.g. early capsule penetration, dia- phragm invasion, differentiation of histological sub- types, etc.

Pancreas

There is little reported information on MRI of the pediatric pancreas. However, in adult patients, MR has been shown to be useful in staging pancreatic neoplasms and the post-operative pancreas [32]. In

T.M. Harris and M. D. Cohen: Abdominal M RI

our experience, fatty replacement of the pancreas in cystic fibrosis is well seen although the clinical value of this finding is questionable.

Spleen

Splenic evaluation with MR remains limited. T1 weighted images generally demonstrate that the nor- mal spleen is isointense with liver. The spleen becomes hyperintense to liver on T2 weighted im- ages. SE imaging of patients with sickle-cell anemia has shown decreased intensity of the spleen com- pared to liver and paraspinal muscles on T2 weighted scans. Calculated T1 and T2 relaxation times are shorter than in normal spleen [33]. These findings are presumably due to iron deposition which causes shortening of T1 and T2 relaxation times. In a case of Hodgkins disease involving the spleen, T1 weighted SE images have shown in- creased intensity of the spleen compared to liver [34]. Splenic abscesses have been imaged demonstrating prolonged T1 and T2 relaxation times (Fig. 12).

Pelvis

MR has been used successfully to identify unde- scended testes in both inguinal and intraabdominal regions [35]. Optimal imaging planes are transaxial

regions [35]. Optimal imaging planes are transaxial Fig.14a-c. Diagnosis: Blood-filled uterine duplication in a
regions [35]. Optimal imaging planes are transaxial Fig.14a-c. Diagnosis: Blood-filled uterine duplication in a

Fig.14a-c. Diagnosis:Blood-filled uterine duplication in a twelve- year-old female, a Transverse sonogram of pelvis demonstrates two rounded fluid-filled structures (arrows) posterior to bladder (b). b and e SE 26/900 Axial and coronal T1 weighted images show oval blood-filled structures with a central septum

Fig,15a and b. Diagnosis:Wilm's tumor, a SE 32/550 Poor bowel opacification makes determination of the exact margins of the fight renal mass (a) difficult on this T1 weighted image. b SE 120/2000 Increased signal from the tumor mass (a) on T2 weighted image makes delineation of tumor from low signal liver (L) and unopacified bowel easier. Gallbladder (G)

T. M. Harris and M. D. Cohen: Abdominal MRI

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T. M. Harris and M. D. Cohen: Abdominal MRI 17 Fig.16a-d. Diagnosis: Multilocular cysticnephroma, a CT
T. M. Harris and M. D. Cohen: Abdominal MRI 17 Fig.16a-d. Diagnosis: Multilocular cysticnephroma, a CT

Fig.16a-d. Diagnosis:Multilocular cysticnephroma, a CT s can shows large fluid den- sity abdominal mass with multiple loculations (arrowheads). b and c SE 40/800 Coro- nal imagesdemonstrate origin of mass (arrow)from upper pole of left kidney (K). Note superior bowel (B) opacification (increased signal)in this patient who had ingested apple juice two hours prior to the scan. d SE 80/2000 T2 weightedimage again shows good bowel delineation (B) and increased signal of well-definedrenal mass (M)

and coronal. Decreased signal on T2 weighted im- ages and smaller size compared to a coexisting nor- mal testis may indicate atrophy. Ano-rectal anom- alies can be demonstrated with MR and multiplanar imaging has been found to be useful in the preopera- tive and postoperative evaluation of the levator sling (Fig. 13) [36, 37]. Uterine anomalies have been evalu- ated with successful demonstration of bicornuate, septate, unicornuate, and didelphys anomalies (Fig. 14) [381.

Bowel

Opacification of the bowel such that it can be distin- guished from other normal intraabdominal organs and abdominal pathology remains a problem in MR

organs and abdominal pathology remains a problem in MR Fig.17. Diagnosis: Respiratory motion artifact and poor

Fig.17. Diagnosis:Respiratory motion artifact and poor bowel opacification. SE 32/500 Respiratory motion on this upper ab- dominal image creates ghosting artifact seen as semicircular bands (arrow) in the phase encoding direction and general blurri- ness of image.Coupled with poor bowel opacification,separation of central retroperitoneal structures from bowel is difficult

(Fig. 15). To data oral contrast agents giving repro- ducible results are not commercially available. Oral iron solutions were initially thought promising but success has been limited. A recent report by Hahn has demonstrated good bowel delineation in rats with ferrite particles [39]. Oral gd-DTPA is also undergoing evaluation [40]. In a recent case at our own institution a child given no oral contrast demon- strated exquisite bowel opacification (Fig. 16). It was later discovered that he had consumed apple juice prior to the examination. Unfortunately, the results were not reproducible in other humans.

Technique

One difficulty encountered in MRI of the abdomen is that of artifacts due to motion. The motion arises from respiration (Fig.17), cardiac pulsation trans- mitted through the diaphragm, aortic pulsation, and bowel peristalsis. Of these causes of motion, the most important is respiration. There are many differ- ent methods that have been tried in order to over- come the effects of respiratory motion. Respiratory gating has not been found to be very effective, as it greatly increases scan time. Breath holding is im- practical, particularly in the pediatric population. Multiple signal averaging increases total scan time but will, to some extent, smooth out the effects of motion. Phase reordering is a complex computer manipulation and at the present time is available only for single slice images and therefore not practi-

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cal. Nonlinear magnetic field gradients greatly help to overcome motion artifacts. They do however re- quire the use of long TE and TR times, which means they are best used for T2 imaging. A simple way of improving respiratory artifacts is to ensure that the phase encoding axis is in the side-to side plane. This helps to decrease the artifact from motion of the anterior abdominal wall. One of the best methods of reducing motion artifact is to reduce the scan time. Using pulse sequences with very short TE (less than 20 msec) and short TR (less than 400 msec) greatly helps to reduce the effects of motion. Field echo im- aging which permits even shorter acquisition times may also, in the future, prove to be helpful in over- coming motion artifacts.

Conclusion

The abdomen remains a difficult area of the body to evaluate with MR. Confounding factors include motion artifact from cardiac pulsation, respiration and bowel peristalsis which degrade image quality. Poor ability to precisely delineate bowel and distin- guish bowel from pathology continues to be a prob- lem. MR has yet to consistently provide unique infor- mation which alters patient management and which is not available by a combination of other imaging modalities. Although MR has the potential to replace multiple-modality imaging in certain cases, rarely does a patient arrive at the scanner without a number of these less sophisticated radiographic studies. At this time a cost savings is only theoretical. We must also remember that we are imaging patients not only to make a diagnosis but in order to convey diagnostic points to clinical collegues. Surgeons and pediatri- cians at our institution seem to be comfortable with conventional imaging modalities (US, CT, EU), rare- ly requesting abdominal MR for routine clinical use. MR is capable of identifying a wide range of patho- logical processes in the abdomen and image quality is continually improving. With few exceptions (e.g. evaluation of levator muscles) MR has not yet been shown to be the imaging modality of first choice in the abdomen and pelvis. Further studies with large num- bers of patients are still needed.

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Received: 22 June 1988; accepted: 1 November 1988

Dr. M. D. Cohen Director Pediatric Radiology Indiana University, School of Medicine 702 Barnhill Drive Indianapolis, IN 46223 USA

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