1816 BALL AJNR: 18, November 1997

Acknowledgment 7. Seltzer SE, Holman BL, Thrall JH, et al. Academic Radiology in a networked environment. Acad Radiol 1996;3:865–872 I gratefully acknowledge the support of Janet L. Strife, 8. Hanks GE. The effects of health care reform on academic medical my chairperson, who has done much to support the con- centers: 1994 gold medal address. Int J Radiat Oncol Biol Phys cepts contained in this report, who recognizes the need for 1995;31:999–1004 change, and who is optimistic about the eventual success 9. Bragg DG, Hendee WR. Support for biomedical research and its of these proposals. impact on radiology. Radiology 1994;193:599–603 10. Matherlee KR. The outlook for clinical research: impacts of federal funding restraint and private sector reconfiguration. Acad Med 1995;70:1065–1072 References 11. Kirks DR. The critical roles of research and education in health 1. Drake DF. Managed care: a product of market dynamics. JAMA care system reform. Acad Radiol 1994;1:293–294 1997;277:560–563 12. Alazraki N. Clinical practice versus research: how can radiology 2. Hillman BJ. Whose turf is imaging? Independent practice, aca- win? Invest Radiol 1993;28:985–986 demics and research. AJR Am J Roentgenol 1991;156:443–447 13. James AE Jr, Partain CL, Heller RM, Patton JA, Price RR. Can 3. Friedman PJ. The impact of health care reform on academic we administrate academics? Preserving the biomedical re- radiology. Invest Radiol 1994;29:790–796 search enterprise in medical imaging. Invest Radiol 1989;24:815– 4. Holman BL. The changing face of academic radiology: can it 816 survive managed care. Acad Radiol 1995;2:1011–1015 14. Staab EV, Langland-Orban B, Gapenski LG. Survey of overhead 5. Friedenberg RM. Medical education and practice in a new envi- assessments of academic health center radiology departments. ronment. Radiology 1997;202:33A–36A Acad Radiol 1994;1:276–282 6. Gallin JI, Smits HL. Managing the interface between medical 15. Hillman BJ, Fajardo LL, Witzke DB, Cardenas D, Irion M, Fulginiti schools, hospitals, and clinical research. JAMA 1997;277:651– JV. Factors influencing radiologists to choose research careers. 654 Invest Radiol 1989;28:842–848

The Encephalopathic Neonate: Choosing the Proper Imaging Technique

A. James Barkovich, University of California, San Francisco

The central nervous system (CNS) of the neonate may Although the value of high-quality neuroimaging in the be injured by a number of different mechanisms, including assessment of the neonate who has suffered an insult to , hypoxia-ischemia, hypoglycemia, hyperbil- the CNS has been generally well accepted, the choice of irubinemia, inborn errors of metabolism, and neonatal in- neuroimaging study has not. Some radiologists rely pri- fections. Neurologic assessment of affected neonates in- marily on transfontanelle sonography while others advo- cludes evaluation of alertness level, cranial nerve function, cate the use of computed tomography (CT) or magnetic motor function (tone, posture, motility, power, and reflex- resonance (MR) imaging techniques. The purpose of this es), presence of neonatal reflexes (Moro, palmar grasp, report is to review briefly the literature on neonatal neuro- and tonic neck response), and gross sensory examination. imaging and to propose a logical approach. However, because of the immaturity of the CNS, neonatal neurologic assessment tests only the function of the brain stem and basal ganglia. Abnormal findings will alert the Techniques clinician to the fact that the infant has suffered a CNS Sonography injury. The precise cause of injury and the severity, extent, and location of the injury to the cerebral cortex are difficult Because the anterior fontanelle of the neonate is usually to establish on clinical grounds. Neuroimaging plays an large, nearly the entire brain can be seen with transfonta- essential role in the assessment of brain injury in these nelle sonography. The ultrasound machine is portable, so patients by helping to establish the cause of injury and the it can be used at the bedside in the neonatal intensive care expected neurologic outcome. unit and obviates transporting the sick infant. Sonography

Address reprint requests to A. James Barkovich, Neuroradiology Section, Room L-371, University of California, San Francisco, 505 Parnassus Ave, San Francisco, CA 94143. Index terms: Brain, diseases; Infants, newborn; Special reports AJNR 18:1816–1820, Nov 1997 0195-6108/97/1810–1816 © American Society of Neuroradiology AJNR: 18, November 1997 CONTROVERSIES 1817 is particularly useful in the imaging of premature neonates, undergoing necrosis followed by cavitation and then who have small brains and unstable circulatory systems. shrinkage of the cavity with resultant focal enlargement of Moreover, the availability of Doppler sonography has the adjacent ventricle (20, 21). PVL should be suspected added a new dimension to the arsenal of the sonographer, when increased echogenicity is present in the periventricu- who can detect altered resistive indexes in neonates who lar regions on sonographic studies; however, edema also have suffered hypoxic-ischemic injury (1–3). causes increased echogenicity and it can resolve without any subsequent (22). Moreover, increased echogenicity can be seen in this region in the absence of CT PVL or edema (23) and normal sonograms have been CT is more useful in older children than in neonates. reported in infants subsequently proved to have PVL at The main reason for the limited utility in neonates is the autopsy (24, 25). Therefore, the appearance of hyperecho- high water content of the neonatal brain, which reduces genicity in itself is not enough to make a diagnosis of PVL. contrast between normal and injured tissue. CT is least The best early sonographic sign of periventricular white useful in premature neonates, in whom white matter injury matter injury is the periventricular “flare,” a globular area is most common; it is more useful in term neonates, who that has echogenicity equal to or greater than that of the are more likely to have suffered gray matter injury (4–6). choroid plexus. If prolonged periventricular flares are seen, In terms of the difficulty of examination, CT is intermediate the prevalence of or tetraplegia can be as between sonography and MR imaging. The patient must be high as 50% (26). A definitive diagnosis of periventricular moved to the CT suite, but is easily monitored during the leukomalacia by sonography requires demonstration of examination and standard life-support equipment is easily cavitation and the subsequent formation of periventricular accommodated in the modern CT suite. cysts (27–31). Cavitation occurs 2 to 6 weeks (usually less than 3 weeks) after injury (31). Although it has been reported that patients with large periventricular cysts MR (more than 5 mm in diameter) have a poorer motor out- MR imaging and MR spectroscopy are probably the come than those with smaller cysts (26), it is wise to most sensitive and specific imaging techniques in the ex- remember that the size of the cysts varies over time; they amination of neonates with suspected brain injury. White enlarge as cavitation develops, and then rapidly shrink matter and gray matter injuries can be detected with MR (21). As a result of the rapid and continuous change in cyst imaging in both term and preterm neonates (5, 7–11). In size, it is probably unwise to rely too heavily on this mea- addition, abnormalities detected on MR studies have pre- surement in predicting outcome. Moreover, it is important dictive value for neurodevelopmental outcome (8, 12, 13). to remember that mildly or moderately injured tissue may Proton MR spectroscopy (14, 15) and diffusion MR imag- not cavitate yet can still cause neurologic deficit (32). ing (16) are useful adjuncts to routine MR imaging and can Other causes of neurologic impairment in premature be acquired with only minimal additional imaging time. neonates, such as infection, infarction, and malformation, However, MR imaging requires transporting infants who may be diagnosed with variable confidence at sonogra- are often hemodynamically unstable. Moreover, special phy. Congenital infections are suggested by the presence life-support and monitoring equipment are needed to per- of lenticulostriate vasculopathy (33, 34); however, this form MR imaging safely on unstable neonates (17). finding is nonspecific (33). Large cortical infarctions are easily diagnosed as triangular regions of hyperechogenic- ity; smaller, more posterior infarctions are more difficult to Recommendations detect. Midline malformations are more easily diagnosed than those occurring more laterally. In spite of its limita- Premature Infants tions, the bedside availability of sonography makes it an Premature infants are often hemodynamically unstable; invaluable tool in the diagnosis of conditions requiring therefore, transporting them is somewhat risky. Transfon- rapid intervention, such as hydrocephalus and hemato- tanelle sonography can be performed in the neonatal in- mas. tensive care unit without moving the neonate and is there- Owing to the low sensitivity of sonography in the de- fore the initial imaging study of choice in all premature tection of nonhemorrhagic, noncavitary parenchymal in- neonates with definite or suspected neurologic impair- jury, another imaging study is usually necessary if the ment. Such techniques as color Doppler sonography and neurologic status of a child is worse than can be explained quantitative sonographic feature analysis (18) may ulti- by sonographic findings. In our experience, CT is not sig- mately result in improved detection of parenchymal injury nificantly more sensitive than sonography for the detection and make the use of other techniques unnecessary. How- of nonhemorrhagic brain injury in premature neonates. ever, sonography is not very sensitive to the detection of The relatively low contrast sensitivity of CT is exacerbated nonhemorrhagic parenchymal injury. Periventricular leu- by the high water content of the premature brain, making komalacia (PVL) has been shown pathologically in 85% of white matter injury (the most common brain injury in pre- infants with birth weights between 900 and 2200 g who mature neonates) very difficult to identify. Because of the survived beyond 6 days (19). The periventricular lesions limitations of CT, MR imaging is recommended as the show a characteristic evolution, with the injured regions neuroimaging study of choice after sonography. Standard 1818 BARKOVICH AJNR: 18, November 1997

MR imaging has much higher contrast resolution and can access to the neonate is maintained during a CT scan. CT unequivocally detect brain injury (manifested as T1 and may show low attenuation in affected gray matter, such as T2 shortening of affected brain parenchyma) within 2 to 3 the thalami, basal ganglia, or cerebral cortex in asphyxi- days of injury (11, 12), before cavitation develops, and, ated neonates. Unfortunately, no studies showing a good therefore, significantly earlier than sonography. MR imag- correlation of CT appearance during the acute phase of ing can be performed safely if chemical blankets are used injury with neurodevelopmental outcome have been pub- to keep the neonate warm and nonparamagnetic or prop- lished; correlations in published studies have not been erly shielded equipment is used. MR imaging is likely to precise, indicating only a gross relationship between the become more sensitive to early injury as diffusion imaging amount of brain damage and patient outcome (37–40). In and spectroscopy become more widely available. these studies, CT suffered from poor detection of both In summary, the initial imaging study in premature ne- subtle damage and developmental malformations. There- onates should be sonography because it is portable and fore, CT is often not helpful in assessing the term neonate. shows most injuries that require immediate intervention. In It may be of some use if high-quality MR imaging is not those patients in whom sonographic findings are inconsis- available and if sonographic findings do not explain the tent with the clinical neurologic examination, MR studies neurologic status of the affected child. should be obtained. MR imaging has the disadvantage of requiring extensive mobilization of the neonatal intensive care unit and radi- ology personnel in order to image a sick neonate safely. Term Infants Special MR-compatible equipment must be acquired and Sonography may be useful as the initial neuroimaging used both for monitoring and for delivering medication to study in the examination of term infants with suspected the infant (17). However, if the departments of neonatol- brain injury. As in preterm infants, sonography detects ogy and radiology are willing to make the necessary effort, large space-occupying masses and hemorrhages that re- high-quality MR images give the most information about quire immediate intervention. The presence of a “feature- the severity of brain damage in the asphyxiated neonate in less brain” (poor gray–white differentiation and effaced the early postnatal period. On day 1, edema can be seen sulci) and increased parenchymal echogenicity is evi- on diffusion-weighted images (16) and on the first echo of dence of diffuse cerebral edema and probable brain injury T2-weighted images; these findings are predictive of poor (35). In perinatal hypoxia-ischemia, the presence of hy- outcome (12). Increased levels of lactate, which are pre- perechogenic basal ganglia or cystic degeneration of the dictive of poor outcome as well (14, 41), can be identified white matter is predictive of poor outcome (8, 36). How- with proton MR spectroscopy within the first few hours of ever, as many as 50% of neurosonograms in neonates with life (15). T1 shortening develops in injured structures hypoxic-ischemic encephalopathy are normal (3); this within 2 to 3 days and T2 shortening within 6 to 7 days percentage is almost certainly higher in neonates with (11). Other than areas of subtle T1 shortening in the basal brain injury resulting from causes other than , ganglia, which are of uncertain long-term prognostic value such as trauma, , and meningitis. The use of (8), these MR abnormalities show excellent correlation Doppler increases the sensitivity and specificity of sonog- with neurodevelopmental outcome (12, 13). Finally, the raphy in asphyxiated neonates, as low resistive indexes in evolution of changes on T1- and T2-weighted images are the anterior and middle cerebral arteries are strong evi- well enough established to allow determination of the time dence of hypoxic-ischemic injury and are predictive of of injury from an MR study obtained in the first few days of poor outcome (1–3). However, Doppler sonographic stud- life; this timing can have important medicolegal implica- ies have not proved to be as sensitive for other causes of tions. neonatal brain injury. In addition, sonography and Doppler In addition to its utility in the assessment of hypoxic- sonography both lack the specificity afforded by recogni- ischemic injury, MR imaging allows evaluation of the entire tion of patterns of injury on MR images. Moreover, sonog- brain, extraparenchymal spaces, and spine, so that pat- raphy has low sensitivity to cortical injuries over the cere- terns of injury can be identified and used to establish a bral convexities, as it is difficult to angle the transducer diagnosis. The entirety of the cerebral cortex is well seen sufficiently to see those areas; focal infarctions, watershed with by MR imaging, so focal infarctions, watershed infarc- injuries, and parietooccipital injury consequent to hypo- tions, and parietooccipital cortical injury consequent to glycemia are, therefore, difficult to detect. Furthermore, hypoglycemia can be easily identified. In addition, the sonography suffers from being highly operator dependent, cerebellum and brain stem, which are difficult to evaluate a situation compounded by the fact that the operator is by sonography because of their distance from the anterior often a technologist who may not be familiar with the fontanelle, are well seen by MR imaging. The many avail- pathophysiology of neonatal brain injury. Finally, if the able MR sequences and the exquisite contrast sensitivity of scan is not performed properly, deliberation with a more MR imaging add to specificity. For example, gradient-echo experienced consultant may not be fruitful. imaging allows precise identification of specific parenchy- CT has the disadvantage of requiring transportation of mal substances, such as blood. T1-weighted images can the sick neonate. However, sedation is not required for CT, show the high-intensity signal of bilirubin in the globi pal- especially if modern scanners with 1- and 2-second scan ladi in patients with kernicterus. Finally, MR angiography time are available. In addition, adequate monitoring and allows the identification of vascular lesions that may have AJNR: 18, November 1997 CONTROVERSIES 1819 led to or stroke and may obviate catheter angiog- Early detection of cerebral infarction and hypoxic ischemic en- raphy (42). cephalopathy in neonates using diffusion weighted magnetic res- In summary, it is always prudent to obtain a sonogram onance imaging. Neuropediatrics 1994;25:172–175 as the initial study in a sick neonate. However, if a lack of 17. Barkovich AJ. Techniques and methods in pediatric imaging. In: concordance is discovered between the clinical course or Pediatric Neuroimaging. 2nd ed. Philadelphia, Pa: Lippincott- Raven; 1995:1–8 the neurologic examination and the sonogram, an MR 18. Barr LL, McCullough PJ, Ball WS, Krasner BH, Garra BS, Deddens study should be obtained if possible, even in the acute JA. Quantitative sonographic feature analysis of clinical infant phase. In the subacute or chronic phase, MR imaging is the hypoxia: a pilot study. AJNR Am J Neuroradiol 1996;17:1025– study of choice to determine the full extent of neurologic 1031 malformation or injury. 19. Shuman RM, Selednik LJ. Periventricular leukomalacia: a one year autopsy study. Arch Neurol 1980;37:231–235 References 20. Volpe JJ. Hypoxic-ischemic encephalopathy: neuropathology and pathogenesis. In: Neurology of the Newborn. 3rd ed. Phila- 1. Gray PH, Tudehope DI, Masel JP, et al. Perinatal hypoxic-isch- delphia, Pa: Saunders; 1995:279–313 aemic brain injury: prediction of outcome. Dev Med Child Neurol 21. Marret S, Mukendi R, Gadisseux J-F, Gressens P, Evrard P. Effect 1993;35:965–973 of ibotentate on brain development: an excitotoxic mouse model 2. Levene MI, Fenton AC, Evans DH, Archer LNJ, Shortland DB, of microgyria and posthypoxic-like lesions. J Neuropathol Exp Gibson NA. Severe birth asphyxia and abnormal cerebral blood Neurol 1995;54:358–370 flow velocity. Dev Med Child Neurol 1989;31:427–434 22. Vannucci RC, Christensen MA, Yager JY. Nature, time-course, 3. Stark JE, Seibert JJ. Cerebral artery Doppler ultrasonography for and extent of cerebral edema in perinatal hypoxic-ischemic brain prediction of outcome after perinatal asphyxia. J Ultrasound Med damage. Pediatr Neurol 1993;9:29–34 1994;13:595–600 23. Grant EG, Schellinger D, Richardson JD, Coffey ML, Smirnioto- 4. Barkovich AJ, Truwit CL. MR of perinatal asphyxia: correlation of poulous JG. Echogenic periventricular halo: normal sonographic gestational age with pattern of damage. AJNR Am J Neuroradiol finding or neonatal cerebral hemorrhage? AJNR Am J Neuroradiol 1990;11:1087–1096 1983;4:43–46 5. Barkovich AJ, Sargent SK. Profound asphyxia in the preterm 24. Dipietro MA, Brody BA, Teele RL. Periventricular echogenic infant: imaging findings. AJNR Am J Neuroradiol 1995;16:1837– “blush” on cranial sonography: pathologic correlates. AJNR Am J 1846 Neuroradiol 1986;7:305–310 6. Barkovich AJ. MR and CT evaluation of profound neonatal and 25. Baarsma R, Laurini RN, Baerts W, Okken A. Reliability of sonog- infantile asphyxia. AJNR Am J Neuroradiol 1992;13:959–972 raphy in non-hemorrhagic periventricular leucomalacia. Pediatr 7. Schouman-Clays E, Henry-Feugeas M-C, Roset F, et al. Periven- Radiol 1987;17:189–191 tricular leukomalacia: correlation between MR imaging and au- 26. Fazzi E, Orcesi S, Caffi L, et al. Neurodevelopmental outcome at topsy findings during the first 2 months of life. Radiology 1993; 5–7 years in preterm infants with periventricular leukomalacia. 189:59–64 Neuropediatrics 1994;25:134–139 8. Rutherford MA, Pennock JM, Dubowitz LMS. Cranial ultrasound 27. Carson SC, Hertzberg BS, Bowie JD, Burger PC. Value of sonog- and magnetic resonance imaging in hypoxic-ischemic encepha- lopathy: a comparison with outcome. Dev Med Child Neurol 1994; raphy in the diagnosis of intracranial hemorrhage and periven- 36:813–825 tricular leukomalacia: a postmortem study of 35 cases. AJNR 9. Keeney SE, Adcock EW, McArdle CB. Prospective observations of Am J Neuroradiol 1990;11:677–684 100 high-risk neonates by high field (1.5 Tesla) magnetic reso- 28. Paneth N, Rudelli E, Monte W, et al. White matter necrosis in nance imaging of the central nervous system, I: intraventricular verylow birth weight infants: neuropathologic and ultrasono- and extracerebral lesions. 1991;87:421–430 graphic findings in infants surviving six days or longer. J Pediatr 10. Keeney S, Adcock EW, McArdle CB. Prospective observations of 1990;116:975–984 100 high-risk neonates by high field (1.5 Tesla) magnetic reso- 29. Sauerbrei EE. Serial brain sonography in two children with leu- nance imaging of the central nervous system, II: lesions associ- komalacia and . J Can Assoc Radiol 1984;35:164– ated with hypoxic-ischemic encephalopathy. Pediatrics 1991;87: 167 431–438 30. Schellinger D, Grant EG, Richardson JD. Cystic periventricular 11. Barkovich AJ, Westmark KD, Ferriero D, Sola A, Partridge C. leukomalacia: sonographic and CT findings. AJNR Am J Neuro- Perinatal asphyxia: MR findings in the first 10 days. AJNR Am J radiol 1984;5:439–445 Neuroradiol 1995;16:427–438 31. Dubowitz LMS, Bydder GM, Mushin J. Developmental sequence 12. Barkovich AJ, Hajnal BL, Vigneron D, et al. MR of perinatal of periventricular leukomalacia: correlation of ultrasound, clinical, asphyxia: new scoring systems utilizing T1-weighted, T2- and nuclear magnetic resonance functions. Arch Dis Child 1985; weighted and contrast-enhanced MR images in the prediction of 60:349–355 neuromotor outcome. AJNR Am J Neuroradiol (in press) 32. 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The Roles of MR Angiography, CT Angiography, and Sonography in Vascular Imaging of the Head and Neck

Michael Brant-Zawadzki, Hoag Memorial Hospital Presbyterian, Newport Beach, Calif, and Joseph E. Heiserman, Barrow Neurological Institute, Phoenix, Ariz

Studying the cervicocranial vasculature in a noninva- cervical carotid bifurcation; specifically, the screening for sive fashion has been a major focus of imaging technology and evaluation of occlusive disease in this region. The for some time. Over the past two decades, a number of concept of a diagnostic screening examination assumes new imaging techniques have been developed and applied the presence of a pathologic process widespread in the to this purpose. Some, like intravenous digital subtraction population that, if detected early, can be arrested or re- angiography, have failed to meet the test of utility despite versed, thus avoiding the otherwise likely consequences of their feasibility. By the mid-1990s, however, at least three severe morbidity and, presumably, improving outcomes, methods of noninvasive imaging have been refined to the as well as (one hopes) saving money in the process. Ath- degree that they now rival conventional intraarterial an- eromatous disease of the carotid bifurcation is just such a giography in accuracy (at least in limited segments of the pathologic process. The potential consequences of stroke anatomy). Magnetic resonance (MR) angiography, Dopp- caused by this entity are significant. Approximately ler sonography, and, most recently, computed tomo- 500 000 Americans suffer from stroke each year. It is the graphic (CT) angiography are now robust techniques. MR third leading cause of death and the leading cause of angiography and Doppler sonography have already disability in the United States. Approximately 40% of all achieved wide popularity, while the growth of CT angiog- ischemic strokes are due to large-vessel disease, particu- raphy has been limited by the relatively slow introduction larly that found at the bifurcation of the internal carotid of slip-ring CT technology, its dependence on intravenous artery. The prevalence of significant carotid bifurcation bolus injection of iodinated contrast material, and the pre- stenosis in the age group at risk for stroke is approximately existing presence of two formidable rivals in the field. The 5% for asymptomatic and 30% for symptomatic persons actual use of these powerful new tools has been propelled most recently by the results of several clinical trials that (1). have changed the approach to patients with carotid occlu- Although trials in the late 1960s and early 1970s sive disease, thus greatly expanding the need for neuro- doused the enthusiasm for surgical intervention in carotid vascular imaging. occlusive disease, recently completed trials have demon- strated considerable improvement in the surgical morbid- ity and mortality of endarterectomy. Such trials have now Cervical Carotid Imaging proved the usefulness of modern carotid endarterectomy The widest use of noninvasive vascular imaging tech- techniques as compared with the best medical therapy in niques has been their application to the evaluation of the the prevention of stroke. The North American Symptom-

Dr Heiserman is the recipient of a grant from the Arizona Disease Control Research Commission. Address reprint requests to Michael Brant-Zawadzki, MD, Department of Radiology, Hoag Memorial Hospital Presbyterian, 1 Hoag Dr, Box 6100, Newport Beach, CA 92658. Index terms: Computed tomography; three-dimensional; Magnetic resonance angiography; Ultrasound; Special reports AJNR 18:1820–1825, Nov 1997 0195-6108/97/1810–1820 © American Society of Neuroradiology