PEDIATRIC NEURORADIOLOGY

The history of any subspecialty in the field of neuroradiology is often determined by the prominence of personal figures who contributed to and shaped its creation. There is little doubt that pediatric neuroradiology has flourished, in part, because of the contributions of individuals such as Harwood-Nash, Naidich, Fitz, Zimmerman, and Barkovich, to name but a few. But it is the literary history of a subspecialty that truly defines its character for all individuals outside of neuroradiology, and that provides definitive evidence of the contribution of a subspecialty to all of neuroscience. In this regard, the AJNR, since its inception in 1980, has played a significant role in defining and shaping the subspecialty of pediatric neuroradiology. During the past 20 years, the AJNR has chronicled a remarkable change in how we image children.

The First 5 Years (1980–1984)

The Golden Age of Sonography and CT

I was surprised to find, when undertaking this assignment, that the first 5 years of pediatric neuroimaging in the AJNR were not defined by conventional angiography, pneumoencephalography, or ventriculography, as we might expect, but rather by sonography and CT. No less than approximately one third of the major articles in this early period related to the use of neurosonography for the evaluation of the neonatal and infant brain and spine. This may be surprising to some, but clearly defines the importance of neurosonography to all of neuroimaging, which continues even today in the hands of both pediatric neuroradiologists and pediatric radiologists.

Perhaps the historical interest in the use of neurosonography to image neonates and infants is not surprising because, from the very beginning, sonography required minimal or no sedation, was portable, and was without the biological effect of ionizing radiation. Whatever the reasons, neurosonography helped shape the literary heritage of pediatric neuroradiology as much as any other imaging technique in use then or today.

The first article in the AJNR on neurosonographic applications was published in 1980. Appropriate to pediatrics and using what then were state-of-the-art static B-mode scanners, it centered on the evaluation of congenital abnormalities of the brain. Oddly enough, CT, also new at that time, was quoted as the standard of reference despite its own recent introduction to the field of neuroimaging. This article was also noteworthy in its reference to the use of neurosonography for sequentially following ventricular dilatation in the neonate, which eventually was to become a frequent use of sonography. This article was soon to be followed by others, which defined the use of sonography for the evaluation of normal anatomy of the brain, the infant cranium, and congenital vascular malformations. It was, however, a series of articles on the use of sonography for diagnosing and following intracranial hemorrhage (ICH) and its complications in the neonate that was to contribute most to the use of sonography in pediatric neuroradiology in these early years. Sonography showed ICH with great sensitivity and specificity and could accomplish this portably as many times as necessary without the use of radiation and at a lower cost. The versatility of neurosonography to diagnose CNS infections and abnormalities of the spine was also introduced to the readership—practices which continue today in the modern neonatal intensive care unit.

In the same period of time, CT began to emerge and significantly impacted the practice of pediatric neuroradiology. CT was to have an even greater impact than sonography owing to the number of children of all age groups it would eventually reach. In a similar fashion to sonography, CT proved very versatile for the evaluation of congenital malformations of the brain, CNS infections, trauma, and primary brain tumors. One of the very first articles to come from the AJNR described the use of CT for evaluating congenital absence of a vertebral pedicle. Articles followed shortly thereafter, showing the superiority of CT over traditional methods of myelography for evaluating congenital malformations of the spine. CT was obviously a natural combination with intrathecal contrast for the evaluation of the cisternal and other CSF spaces. CT was quickly shown to be of value for the intracranial diagnosis and evaluation of primary tumors of the brain and surrounding structures. CT also offered us the ability to image in direct coronal and sagittal projections to see anatomy from perspectives never before realized. The use of CT to evaluate perinatal intracranial hemorrhage compared with pathologic analysis earned Ludwig the Dyke Award during the 1982 annual meeting of the ASNR.

CT further contributed to our understanding and appreciation of two major concepts in pediatric neuroradiology; that of the effect changing development has on the appearance of the child's brain and how the attenuation characteristics of tissue and fluid could be used to assess both congenital and neoplastic processes. In a classic series that was to be repeated many times, investigators revealed how the CT of normal development could be used to assess abnormal cranial development in patients with microcephaly. CT also clearly opened up new vistas in the evaluation of the pediatric spine, and allowed us a look at disease processes previously only seen by the neurosurgeon and pathologist. Classic imaging descriptions of processes such as lipomyeloschisis and primary tethered cord syndrome extended our ability to serve the patient, and extended the influence and respect of pediatric neuroradiology among our clinical colleagues.

The first 5 years also brought to our attention pediatric applications of the new and developing field of neurointervention. The use of embolic methods to treat juvenile angiofibromas was to be described early in the AJNR, and was to be followed in later years by even greater and more complex applications of neurointervention in children.

It was during these early years that we also were first introduced to disorders that previously were only the domain of the pediatrician and neuropathologist. Metabolic disorders of the brain were, until now, read about but seldom seen by the neuroradiologist. CT played an essential role in introducing us to metabolic disorders in these early times—a role that eventually was to be totally replaced by MR imaging. Descriptions of unusual conditions such as fucosidosis, neurofibromatosis, adrenoleukodystrophy, methylmalonic and proprionic acidurias and Krabbe's disease were to enter the vocabulary of the neuroradiologist as CT, and eventually MR imaging, entered the picture.

This was truly an exciting time for pediatric neuroimaging that had built a firm foundation not only for a developing subspecialty, but also for the personal careers of many individuals in pediatric neuroradiology. As this period began drawing to a close in 1984, evidence of an even a greater future in the use of magnetic resonance imaging to diagnose cerebral disorders in children, began taking shape.

The Next Five Years (1985–1989)

The Contribution of MR Takes Shape

This period, as much as any other, truly shaped modern pediatric neuroradiology. This period was the prelude to the decade of the brain and the emergence of MR imaging as the dominant technique in pediatric neuroradiology. The important roles of CT and sonography were not to be lost, however, as can be easily seen as this period began. Rather than to focus on the technical aspects of a technique, imaging began focusing more on disease processes. The diagnostic potential of imaging for characterizing and staging primary brain tumors, such as the primitive neuroectodermal tumor, and determining the effect on tumor patient management. Through CT, we could not only now tell the clinician that a tumor existed, but what its likely histologic characteristics would be. Early recognition of complications related to various disease states were now also possible, which, until now, could only be identified in the very late stages of the disease process. With the use of CT, new and exotic illnesses were defined, such as disorders in neuronal migration, that eventually would emerge as a significant cause of childhood morbidity and mortality. Our vocabulary soon included terms such as lissencephaly and schizencephaly that before were terms only mentioned to us by the developmental pediatrician or the pathologist. It now became obvious that even the neuroradiologist must be able to understand and classify malformations of the brain based on embryologic development. Such classifications, as published in the AJNR of van der Knapp and Valk, were paramount to our understanding of these conditions. The ability to recognize even minor malformations in vivo changed the shape of genetics.

It was, however, the diagnosis and management of intracranial tumors that was to dominate the CT literature during this period of time. Tumors such as choroid plexus papilloma, optic pathway gliomas, and gangliogliomas were regarded very differently based on what was recognized through imaging. An easy way to follow the effect of therapy now emerged through CT, and imaging eventually was to become part of every treatment protocol.

The key to the diagnosis of childhood disease has always been, and always will be, first the recognition of the normal appearance. Not surprisingly, the process of defining normal brain maturation and recognizing variations in brain development as seen by CT, sonography, and, later, MR imaging was the topic of numerous investigations. From asymmetry in the temporal lobes, to the size of the normal pituitary stalk, the normal process of development was further defined through imaging. This process was to become even more important with the emergence of MR imaging, with its improved resolution and ability to reveal not only tissue structure but also characteristics of tissue composition. MR imaging emerged as a new way of following maturation through depicting the T1 and T2 characteristics of myelination. Landmark articles that remain standards of reference were published throughout this 5-year period. No longer was the term “developmental delay” to be determined by physical examination alone. The impact of such contributions was to have a far greater reach than just in neuroradiology, but impacted all of pediatrics.

It was during this period that we also witnessed a significant shift of attention in pediatric neuroimaging techniques. Sonography continued in the first half of this period to play a strong role in pediatric neuroimaging. No less than 20 articles for its use in hemorrhagic disorders in the premature infant, follow-up of neonatal hydrocephalus, and evaluation of infections of the infant brain were to be published in the years 1985–1987. By the end of this period, however, this publication record for sonography fell to only five to eight articles, which were nonetheless important contributions to neuroimaging. Despite this decline, sonography was clearly established in the armamentarium of the neuroradiologist and pediatric radiologist as the principle technique for assessing the preterm infant and the follow-up of neonatal hydrocephalus. CT was also clearly established in the evaluation of the pediatric head and neck, the bony calvarium, and pediatric head trauma, including that secondary to abuse.

By the end of this period, however, it was clear that MR imaging was to become the primary focus of interest in pediatric neuroradiology for the next decade. As early as 1985, MR imaging of the pediatric spine clearly emerged as the primary technique for assessing spinal soft tissue. This included the recognition of malformations of the craniocervical junction, such as the Chiari I malformation, with far greater frequency than was previously recognized. The presence of syringomyelia and hydromyelia of the cord, as well as defects such as diastematomyelia, could easily be recognized by MR imaging without the need for myelography or ionizing radiation. This was to change the very way we screened the pediatric spine for disease. Myelography no longer was to be performed with its previous frequency. Reports in the AJNR regarding the use of spinal MR imaging in children testified to this trend toward less invasive and more accurate diagnoses achieved by MR imaging.

In the time that was to follow, the use of MR imaging to diagnose primary brain tumors, congenital malformations, vascular malformations presenting in childhood, metabolic diseases, and childhood cerebrovascular disease were the focus of numerous contributions to the AJNR. MR imaging was not only a more accurate way to make a diagnosis, but also provided insight into the actual classification and pathophysiology of such malformations, such as dysgenesis of the corpus callosum and disorders of neuronal migration. As in the previous 5-year period when many anatomic abnormalities became “newly” discovered through imaging, MR imaging allowed neuroradiologists to diagnose and recognize many metabolic and neurodegenerative disorders unfamiliar to most. Names like Pelizaeus-Merzbacher disease, Leigh disease, oculocerebrorenal disease, and Menkes disease began cropping up with increasing frequency in journal articles with every issue. We were soon to learn from this experience that conditions such as these were not as rare as previously thought, but only perhaps unrecognized with sufficient frequency. MR imaging was clearly here to stay, and was clearly to remain a significant part of our literary history in the AJNR for the decade to come.

The Decade of the Brain (1990–1995)

The Early Years

With the beginning of the 1990s came the beginning of what was to be referred to as the Decade of the Brain. This period was as productive for pediatric neuroradiology as it was for all of neuroradiology and for the Journal. By 1990, MR was clearly the dominant imaging technique used in pediatric neuroradiology. This period was to continue with the trend of shifting from the technical aspects of imaging to categorizing disease processes. Several relatively new sections were to emerge in the Journal, encompassing some familiar and some not-so-familiar conditions. An entire section was devoted to imaging of the phakomatoses, in part because of the number of good publications submitted and in part owing to the fact that this group of conditions, perhaps more than any other in children, lent itself well to MR imaging. Never before had we realized the scope of CNS involvement in the phakomatoses by diseases such as cutaneous melanosis, neurofibromatosis, epidermal nevus syndrome, Sturge Weber syndrome, and tuberous sclerosis. Rare phakomatoses, such as segmental neurofibromatosis, now approached center stage through publication. Excellent scientific reports introduced us to exotic conditions such as Lhermitte-Duclos disease and linear sebaceous nevus syndrome, allowing readers to recognize them by example.

During this period, acceptance of papers for publication played on the strengths of MR imaging to explore new territories, especially in the area of metabolic and neurodegenerative disease. Reports on the MR imaging findings in phenylketonuria, Refsum disease, glutaric and methylmalonic acidurias emerged that would be joined later by even newer developments in MR spectroscopy. The visual display of such conditions would later play a significant role in their differential characterization. More common conditions, such as the mitochondrial leukodystrophies and Krabbe's disease, were described in sufficient detail to allow their identification by all of neuroradiology and not just a few. As these conditions are very rare and seldom present in a single institution, the publications of high-quality images representing these disorders began to serve as pictorial references for comparison by many investigators as they might encounter them in their own practice. As if to appear in groups by chance, entities such as Kallmann syndrome, with its array of imaging findings, began appearing in a number of excellent descriptive articles. More advanced imaging, such as spectroscopy, also appeared to show promise in the evaluation of neurodegenerative disorders for which anatomic imaging alone still provided incomplete information.

It was, however, in 1992 that the field of pediatric neuroradiology truly came into its own as a subspecialty, with significant literary exposure to the readership of the AJNR. It was the year that Dr. Michael Huckman took two bold steps. The first was to change the appearance of the journal (for the better, I might add). The second was to publish, in its entirety, a symposium on pediatric neuroradiology created by Dr. Thomas Naidich and given by foremost and upcoming experts in the field of pediatric neuroradiology at the 1992 annual meeting of the ASNR. This symposium, perhaps more than any other format at the time, defined the broad scope of what was then pediatric neuroradiology. It also indicated to all in the ASNR and in neuroscience that this subspecialty had finally matured into a significant part of neuroradiology. Volume 13, number 2 was, as published, not just another issue of the Journal, but a concise textbook on pediatric neuroimaging. It remains so even today an excellent source for review and pathologic correlation.

Conditions that were to play a large role in pediatric neuroimaging were the topics of numerous reports published over this period in the AJNR. Migrational disorders were defined to the point of classification based not on pathology, but according to patterns seen on imaging. Neonatal brain imaging advanced to the point that imaging allowed a better definition of the pathologic changes in infants with cerebral palsy and developmental delay. Cocaine abuse and its effect upon the developing brain was just one example of how imaging added to the total body of knowledge within well-defined areas. Most importantly, articles published in the AJNR continued to advance our understanding of how significant brain injury often had its origin in utero, and this understanding was based on recognizable patterns of abnormalities seen with imaging. Imaging began to support the clinical work of clinical pediatric pioneers such as Nelson and Ellenberg who sought to prove that in utero injury was in fact the leading cause of postnatal developmental delay. Neuroradiology responded by many articles in support of this concept.

The anatomic virtues of MR imaging were fully explored over this period. Primary CNS neoplasms in childhood were further characterized to the point of common recognition. Less common tumors in childhood such as meningiomas and oligodendrogliomas were the topics of excellent reports in the AJNR. Although less common than in adults, a literary focus on cerebrovascular disease in children began to emerge after a long hiatus. Congenital malformations such as those found in the region of the vein of Galen were better characterized to allow for specific neuroradiologic intervention. The wide variety of causes of cerebrovascular disease in children such as mitochondrial disease, moyamoya, and aneurysm was becoming more obvious in practice by the increasing number of reports on these and other subjects that were to continue to increase over the next 5 years.

Of particular note was the emergence of a relatively new method to pediatric imaging, that of MR spectroscopy (MRS). Its use in the evaluation of childhood metabolic disorders, and specifically neurodegenerative disease, became the topic of several major articles and short reports. The use of MRS, as opposed to standard laboratory methods, could actually establish the diagnosis for conditions such as nonketotic hyperglycinemia. Other uses of MRS to assess heterotopias and HIV infections in neonates were also published. It was during this time that the AJNR published its first article on the pediatric use of diffusion-weighted MR imaging to assess brain maturation. By the close of this first half of the decade of the brain, anatomic imaging by MR imaging was clearly established, and the stage was set for the next major advance in pediatric neuroradiology, that of imaging brain function as well as form.

The Decade of the Brain (1995–1999)

Prelude to the Future

By 1995, the AJNR clearly led the way in publishing on all aspects of pediatric neuroradiology. MR imaging now was the most often used technique in pediatric neuroimaging, but CT and sonography both maintained well-deserved strong niches for specific clinical indications. It was also clear that we no longer viewed imaging strictly from a technical perspective, but rather as a vehicle to uncover new and important information about the physiology of the pathologic condition. Imaging became firmly entrenched in the management of patients, as it now became a part of almost every treatment protocol to screen for and follow neurologic disease. The focus of the pediatric neuroradiologist was no longer just on diagnosing the presence or absence of a disorder, but rather in uncovering information about its physiology, natural history, and the direct effect treatment had on the underlying pathology. During this period, literary documentation clearly demonstrated that we no longer viewed pathology as purely anatomic in nature, but as a complex process consisting of cellular metabolism, vascular perfusion, and diffusion of water. If literature is to be considered a roadmap of where we are and where we are going, the changing course of pediatric neuroradiology was clearly set in the literary record of this period.

Sonography, which began the first decade in the AJNR with one third of the manuscripts, by the last 5 years had dropped to less than 10 papers. Although the quality of these papers stand as evidence of a strong continued role for sonography in pediatric neuroradiology, I can only say that the numbers of currently submitted sonographic investigations in no way equal those of the past. Although sonography has certainly given way to MR for the imaging of all age groups, it remains a very useful method to evaluate and screen for CNS disease in neonates and infants. Several articles during this period investigated sonography of the infant spine; one of these articles clearly demonstrated a role for sonography in screening the infant spine to identify the level of the conus. Sonography of the brain, like other techiniques, continues to expand its abilities to depict pathophysiologic changes beyond its traditional role of anatomic imaging. In one study, investigators clearly demonstrated the promise of quantitative analysis of the infant brain for the detection of hypoxic-ischemic encephalopathy while maintaining the portability and low cost inherent to this method. Investigators also demonstrated the future of contrast enhancement in sonography in one report on neonatal hydrocephalus. Such advances are likely to continue. Although sonography is not likely to be as widely used in the future as it was in the past, technical advances provide clear evidence that its role, while changing, is likely to remain strong in the neonatal intensive care unit for years to come.

In a similar fashion to sonography, articles reporting the benefits of CT also dramatically declined mostly because of increasing MR imaging. A number of excellent correlative articles were published during this period in which MR and CT scanning were performed in the same subjects. Although these were not direct statistical comparisons, it is clear that a role for CT of the brain, secondary to that of MR imaging, had developed by 1996. CT did, however, solidify its niche in the evaluation of the skull base and cranium, and maintained a hold as well on the evaluation of the pediatric head and neck. Articles defining the normal anatomy of the skull base and larynx were published, and became the anatomic standard for defining both normal and abnormal morphology of these regions in children. CT still proved to be quite useful in the evaluation of the neck for conditions, such as fat necrosis and congenital anomalies of the pediatric spine. By 1999, the hint of new applications for pediatric CT began to emerge, as they did for the imaging of adults, through the application of CT angiography. Helical CT angiography may eventually prove as useful as MR angiography as the range of cerebrovascular disease in children widens and increases in clinical importance.

Nevertheless, it was MR imaging that clearly emerged as the leader in pediatric neuroimaging by the end of the millennium, and it is unlikely that this trend will be altered in the near future. Leading the applications of MR imaging was its continued use for exploring metabolic and neurodegenerative disease in the pediatric age group. The use of MR imaging for evaluating demyelinating disorders, such as multiple sclerosis in children, paralleled its similar use in adults; however, the balance of MR imaging applications in metabolic and neurodegenerative disease in children focused on developmental metabolic defects. MR imaging and advanced methods such as MR spectroscopy were used to study a wide range of conditions, including the phakomatoses, mitochondrial disorders, adrenoleukodystrophy, lysosomal disorders, and Pelizaaeus-Merzbacher disease. MR imaging improved our understanding of the development of many of these conditions as well as provided morphologic information regarding their course. Advanced imaging, such as MR spectroscopy of adrenoleukodystrophy, was shown to be more sensitive than physical examination for following up patients with metabolic diseases. By the end of the decade of the brain, MR imaging and MR spectroscopy had advanced to the imaging method of choice in the evaluation and follow-up of children with a wide variety of metabolic and neurodegenerative diseases.

The role of MR imaging in the evaluation of childhood epilepsy also surged forward in the latter half of the decade. The value of high-resolution imaging for detecting structural causes of epilepsy improved lesion detection. Other reports better defined the range of developmental abnormalities that might contribute to childhood epilepsy by using MR imaging. The multiplanar capabilities of MR imaging also allowed better definition of cortical dysplasias and migrational anomalies that contribute to neurologic disease in the pediatric population.

The importance of understanding normal development and anatomy depicted on MR images led to numerous reports on the subject in the latter half of the decade. Both normal and abnormal development of the temporal lobes were highlighted as examples of what we may still learn from such anatomic investigations. Other reports touched on a wide range of developmental issues, including that of normal formation of the pituitary gland, the operculum, the corpus callosum, the hippocampus, myelination, and supratentorial parenchyma.

Neonatal imaging continued with a strong showing in this period as well. Reports improved our understanding of perinatal asphyxia and its appearance in both the term and preterm infant as well as in neonatal trauma. Kernicterus appeared again to be on the rise after a decrease in previously published reports. The evolution of the germinal matrix hemorrhage was better identified by careful comparison of imaging with the pathologic condition, as was the relationship between structural injury and metabolic conditions, such as neonatal hypoglycemia. More careful analysis of the imaging patterns of birth asphyxia led to the development of image-based scoring systems that may in time prove valuable in the assessment of severity and have improved our ability to predict outcome.

By the close of this period, the use of advanced MR applications such as MR spectroscopy, perfusion, and diffusion set the tone for what neuroradiologists must be capable of understanding if we are to continue as imagers in the future.

In summary, this has been an interesting 20 years of literary growth in pediatric neuroradiology. The publication record of the AJNR shows us where we began and how we got to the beginning of the future. Neuroradiologists developed and defined what is the subspecialty of pediatric neuroradiology. Our literary contributions far surpassed any other literary contributions in pediatric neuroscience. Our future is to be considered bright only if we can continue in this role.

References

Sauerbrei EE, Cooperberg PL. Neonatal brain: sonography of congenital abnormalities. AJNR Am J Neuroradiol 1981;2:125-128
Pigadas A, Thompson JR, Grube GL. Normal infant cranial anatomy: correlated real-time sonograms and brain specimens. AJNR Am J Neuroradiol 1981;2:339-344
Shuman WP, Rogers JV, Mack LA, Alvord EC, Christie DP. Real-time sonographic sector scanning of the neonatal cranium: technique and normal anatomy. AJNR Am J Neuroradiol 1981;2:349-356
Cubberley DA, Jaffee RB, Nixon GW. Sonographic demonstration of galenic arteriovenous malformations in the neonate. AJNR Am J Neuroradiol 1982;3:435-439
Grant EG, Borts F, Schellinger D, McCullough DC, Smith Y. Cerebral intraparenchymal hemorrhage in neonates: sonographic appearance. AJNR Am J Neuroradiol 1981;2:129-132
Albright L, Fellows R. Sequential CT scanning after neonatal intracerebral hemorrhage. AJNR Am J Neuroradiol 1981;2:133-138
Babcock DS, Bove KE, Han BK. Intracranial hemorrhage in premature infants: sonographic-pathologic correlation. AJNR Am J Neuroradiol 1982;3:309-318
Reeder JD, Kaude JV, Setzer ES. Choroid plexus hemorrhage in premature neonates. AJNR Am J Neuroradiol 1982;3:615-618
Fleischer AC, Hutchison AA, Bundy AL. Serial sonography of posthemorrhagic ventricular dilatation and porencephaly after intracranial hemorrhage. AJNR Am J Neuroradiol 1983;4:971-975
Bowie JD, Kirks DR, Rosenberg ER, Clair MR. Caudothalamic groove: value in identification of germinal matrix hemorrhage by sonography in preterm neonates. AJNR Am J Neuroradiol 1983;4:1107-1110
Bowerman RA, Donn SM, Silver TM, Jaffe MH. Review. Natural history of neonatal periventricular/intraventricular hemorrhage and its complications: sonographic observations. AJNR Am J Neuroradiol 1984;5:527-538
Edwards MK, Brown DL, Chua GT. Complicated infantile meningitis: evaluation by real-time sonography. AJNR Am J Neuroradiol 1982;3:431-434
Kangarloo H, Gold RH, Diament MJ, Boechat MI, Barrett C. High-resolution spinal sonography in infants. AJNR Am J Neuroradiol 1984;5:191-195
Lauten GJ. Computed tomography in absent cervical pedicle. AJNR Am J Neuroradiol 1980;2:201-203
Wolpert SM, Scott RM. The value of metrizamide CT cisternography in the management of cerebral arachnoid cysts. AJNR Am J Neuroradiol 1981;2:29-36
Lauten GJ, Eatherly JB, Ramirez A. Hemangioblastomas of the optic nerve: radiographic and pathologic features. AJNR Am J Neuroradiol 1981;2:96-99
Futrell NN, Osborn AG, Cheson BD. Pineal region tumors: computed tomographic-pathologic spectrum. AJNR Am J Neuroradiol 1981;2:415-420
Swenson SA, Forbes GS, Younge BR, Campbell RJ. Radiologic evaluation of tumors of the optic nerve. AJNR Am J Neuroradiol 1982;3:319-326
Armstrong EA, Harwood-Nash DCF, Hoffman H, Fitz CR, Chuang S, Pettersson H. Benign suprasellar cysts: the CT approach. AJNR Am J Neuroradiol 1983;4:163-166
Kaiser MC, Pettersson H, Harwood-Nash DC, Fitz CR, Armstrong E. Direct coronal CT of the spine in infants and children. AJNR Am J Neuroradiol 1981;2:465-466
Hahn FJ, Chu WK, Torkelson RD. CT measurements of cranial growth: microcephaly. AJNR Am J Neuroradiol 1984;5:159-160
Naidich TP, McLone DG, Mutluer S. A new understanding of dorsal dysraphism with lipoma lipomyeloschisis.: radiologic evaluation and surgical correction. AJNR Am J Neuroradiol 1983;4:103-116
Sarwar M, Virapongse C, Bhimani S. Primary tethered cord syndrome: a new hypothesis of its origin. AJNR Am J Neuroradiol 1984;5:235-242
Bryan RN, Sessions RB, Horowitz BL. Radiographic management of juvenile angiofibromas. AJNR Am J Neuroradiol 1981;2:157-166
Kessler RM, Altman DH, Martin-Jimenez R. Cranial CT in fucosidosis. AJNR Am J Neuroradiol 1981;2:591-592
Inoue Y, Fukuda T, Takashima S, et al. Adrenoleukodystrophy: new CT findings. AJNR Am J Neuroradiol 1983;4:951-954
Gebarski SS, Gabrielsen TO, Knake J, Latack JT. Cerebral CT findings in methylmalonic and popionic acidemias. AJNR Am J Neuroradiol 1983;4:955-958
Kwan E, Drace J, Enzmann D. Specific CT findings in Krabbe disease. AJNR Am J Neuroradiol 1984;5:453-458
Peterman SB, Steiner RE, Bydder GM. Magnetic resonance imaging of intracranial tumors in children and adolescents. AJNR Am J Neuroradiol 1984;5:703-710
Johnson MA, Desai S, Hughes-Jones K, Starer F. Magnetic resonance imaging of the brain in Hurler syndrome. AJNR Am J Neuroradiol 1984;5:816-819
Altman N, Fitz CR, Chuang S, Harwood-Nash DC, Cotter C, Armstrong D. Radiologic characteristics of primitive neuroectodermal tumors in children. AJNR Am J Neuroradiol 1985;6:15-18
Lee BCP, Kneeland JB, Cahill PT, Deck MDF. MR recognition of supratentorial tumors. AJNR Am J Neuroradiol 1985;6:871-878
North C, Segall HD, Stanley P, Zee CS, Ahmadi J, McComb JG. Early CT detection of intracranial seeding from medulloblastoma. AJNR Am J Neuroradiol 1985;6:11-14
Babcock DS, Han BK. Sonographic recognition of gyral infarction in meningitis. AJNR Am J Neuroradiol 1985;6:119-122
Dobyns WB, McCluggage CW. Computed tomographic appearance of lissencephaly syndromes. AJNR Am J Neuroradiol 1985;6:545-550
Bird CR, Gilles FH. Type I schizencephaly: CT and neuropathologic findings. AJNR Am J Neuroradiol 1987;8:451-454
Barkovich AJ, Chuang SH, Norman D. MR of neuronal migration anomalies. AJNR Am J Neuroradiol 1987;8:1009-1018
van der Knaap MS, Valk J. Classification of congenital abnormalities of the CNS. AJNR Am J Neuroradiol 1988;9:315-326
Chow PP, Horgan JG, Burns PN, Weltin G, Taylor KJW. Choroid plexus papilloma: detection by real-time and Doppler sonography. AJNR Am J Neuroradiol 1986;7:168-170
Dorne HL, Lander PH. CT recognition of anomalies of the posterior arch of the atlas vertebrae: differentiation from fracture. AJNR Am J Neuroradiol 1986;7:176-177
Seidenwurm D, Bird CR, Enzmann DR, Marshall WH. Left-right temporal region asymmetry in infants and children. AJNR Am J Neuroradiol 1985;6:777-780
Seidel FG, Towbin R, Kaufman RA. Normal pituitary stalk size in children: CT study. AJNR Am J Neuroradiol 1985;6:733-738
Holland BA, Haas DK, Norman D, Brant-Zawadzki M, Newton TH. MRI of normal brain maturation. AJNR Am J Neuroradiol 1986;7:201-208
Dietrich RB, Bradley WG, Zaragoza EJ, et al. MR evaluation of early myelination patterns in normal and developmentally delayed infants. AJNR Am J Neuroradiol 1988;9:69-76
Bird CR, Hedberg M, Drayer BP, Keller PJ, Flom RA, Hodak JA. MR assessment of myelination in infants and children: usefulness of marker sites. AJNR Am J Neuroradiol 1989;10:731-740
Lee BCP, Deck MDF, Kneeland JB, Cahill PT. MR imaging of the craniocervical junction. AJNR Am J Neuroradiol 1985;6:209-214
Altman NRADH. MR imaging of spinal dysraphism. AJNR Am J Neuroradiol 1987;8:533-538
Spinos E, Laster DW, Moody DM, Ball MR, Witcofski RL, Kelly DL. MR evaluation of Chiari I malformations at 0.15 T. AJNR Am J Neuroradiol 1985;6:203-208
Barkovich AJ, Wippold FJ, Sherman JL, Citrin CM. Significance of cerebellar tonsillar position on MR. AJNR Am J Neuroradiol 1986;7:795-800
Barnes PD, Lester PD, Yamanashi WS, Prince JR. Magnetic resonance imaging in infants and children with spinal dysraphism. AJNR Am J Neuroradiol 1986;7:465-472
Sherman JL, Barkovich AJ, Citrin CM. The MR appearance of syringomyelia: new observations. AJNR Am J Neuroradiol 1986;7:985-996
Rhodes RE, Friedman HS, Hatten HP, Hockenberger B, Oakes WJ, Tomita T. Contrast-enhanced MR imaging of neurocutaneous melanosis. AJNR Am J Neuroradiol 1991;12:380-396
Barkovich AJ, Frieden ML, Williams ML. MR of neurocutaneous melanosis. AJNR Am J Neuroradiol 1994;15:859-868
Friedman DP. Segmental neurofibromatosis (NF-5): a rare form of neurofibromatosis. AJNR Am J Neuroradiol 1991;12:971-1028
Yamada K, Ohta T, Miyamoto T. Bilateral trigeminal schwannomas associated with von Recklinghausen's disease. AJNR Am J Neuroradiol 1992;13:299-300
Itoh T, Magnaldi S, White RMeal. Neurofibromatosis type I: the evolution of deep gray and white matter MR abnormalities. AJNR Am J Neuroradiol 1994;15:1513-1520
Lazzeri S, Mascalchi M, Cellerini M, Martinetti MG, Dal Pozzo G. Epidermal nevus syndrome: MR of intracranial involvement. AJNR Am J Neuroradiol 1993;14:1255-1257
Decker T, Jones K, Barnes P. Sturge-Weber syndrome with posterior fossa involvement. AJNR Am J Neuroradiol 1994;15:389-392
Wilms G, Van Wijck E, Demaerel P, et al. Gyriform calcifications in tuberous sclerosis simulating the appearance of Sturge-Weber disease. AJNR Am J Neuroradiol 1992;13:295-298
Williams IDW, Elster AD, Ginsberg LE, Stanton C. Recurrent Lhermitte-Duclos disease: report of two cases and association with Cowden's disease. AJNR Am J Neuroradiol 1992;13:287-290
Cavenagh EC, Hart BL, Rose D. Association of linear sebaceous nevus syndrome and unilateral megalencephaly. AJNR AM J Neuroradiol 1993;14:405-408
Naidu SB, Moser HW. Commentary. Value of neuroimaging in metabolic disease affecting CNS. AJNR Am J Neuroradiol 1991;12:413-416
Shaw DWW, Maravilla KR, Weinberger E, Garretson J, Trahms CM, Scott CR. MR imaging of phenylketonuria. AJNR Am J Neuroradiol 1991;12:403-406
Dubois J, Sebag G, Argyropoulou M, Brunelle F. MR findings in infantile Refsum disease: case report of two family members. AJNR Am J Neuroradiol 1991;12:1159-1160
Andreula CF, De Blasi R, Carella A. CT and MR studies of methylmalonic acidemia. AJNR Am J Neuroradiol 1991;12:410-412
Barkovich AJ, Good WV, Koch TK, Berg BO. Mitochondrial disorders: analysis of their clinical and imaging characteristics. AJNR Am J Neuroradiol 1993;14:1119-1138
Heckmann JM, Eastman R, Handler L, Wright M, Owen P. Leigh disease: (subacute necrotizing encephalomyelopathy): MR documentation of the evolution of an acute attack. AJNR Am J Neuroradiol 1993;14:1157-1159
Finelli DA, Tarr RW, Sawyer RN, Horwitz SJ. Deceptively normal MR in early infantile Krabbe disease. AJNR Am J Neuroradiol 1994;15:167-171
Truwit CL, Barkovich AJ, Grumbach MM, Martini JJ. MR imaging of Kallmann syndrome, a genetic disorder of migration affecting the olfactory and genital systems. AJNR Am J Neuroradiol 1993;14:827-838
Yousem DM, Turner WJD, Li C, Snyder PJ, Doty RL. Kallmann syndrome: MR evaluation of olfactory system. AJNR Am J Neuroradiol 1993;14:839-844
Knorr JR, Ragland RL, Brown RS, Geiber N. Kallmann syndrome: MR findings. AJNR Am J Neuroradiol 1993;14:845-851
Tzika AA, Ball WS, Vigneron DB, Dunn RS, Kirks DR. Clinical proton MR spectroscopy of neurodegenerative disease in childhood. AJNR Am J Neuroradiol 1993;14:1267-1281
Gallucci M, Bozzao A, Curatolo P, Splendiani A, Cifani A, Passariello R. MR imaging of incomplete band heterotopias. AJNR Am J Neuroradiol 1991;12:701-702
Barkovich AJ, Gressens P, Evrard P. Formation, maturation, and disorders of brain neocortex. AJNR Am J Neuroradiol 1992;13:423-446
Castillo M, Bouldin TW, Scatliff JH, Suzuki K. Radiologic-pathologic correlation. Alobar holoprosencephaly. AJNR Am J Neuroradiol 1993;14:1151-1156
Kuzniecky R, Andermann F. The congenital bilateral perisylvian syndrome: imaging findings in a multicenter study. AJNR Am J Neuroradiol 1994;15:139-144
Truwit CL, Barkovich AJ, Koch TK, Ferriero DM. Cerebral palsy: MR findings in 40 patients. AJNR Am J Neuroradiol 1992;13:67-78
Barkovich AJ. MR and CT evaluation of profound neonatal and infantile asphyxia. AJNR Am J Neuroradiol 1992;13:959-972
Brunberg JA, Kewitz G, Schumacher RE. Venovenous extracorporeal membrane oxygenation: early CT alterations following use in management of severe respiratory failure in neonates. AJNR Am J Neuroradiol 1993;14:595-603
Rollins NK, Moriss MC, Evans D, Perlman JM. The role of early MR in the evalution of term infant with seizures. AJNR Am J Neuroradiol 1994;15:231-238
Dogra VS, Shyken JM, Menon PA, Poblete J, Lewis D, Smeltzer JS. Neurosonographic abnormalities associated with maternal history of cocaine use in neonates of appropriate size for their gestational age. AJNR Am J Neuroradiol 1994;15:697-702
Kazam E, Rudelli R, Monte Weal. Sonographic diagnosis of cisternal subarachnoid hemorrhage in the premature infant. AJNR Am J Neuroradiol 1994;15:1009-1020
Heier LA, Carpanzano C, Mast J, Brill PW, Winchester P, Deck MDF. Maternal cocaine abuse: the spectrum of radiologic abnormalities in the neonatal CNS. AJNR Am J Neuroradiol 1991;12:951-956
Mamourian AC, Lewandowski AE, Towfighi J. Cystic intraparenchymal meningioma in a child: case report. AJNR Am J Neuroradiol 1991;12:366-367
Hope JKA, Armstrong DA, Babyn PSeal. Primary meningeal tumors in children: correlation of clinical and CT findings with histologic type and prognosis. AJNR Am J Neuroradiol 1992;13:1353-1364
Glasier CM, Husain MM, Chadduck W, Boop FA. Meningiomas in children: MR and histopathologic findings. AJNR Am J Neuroradiol 1993;14:237-241
Darling CF, Byrd SE, Reyes-Mugica M, et al. MR of pediatric intracranial meningiomas. AJNR Am J Neuroradiol 1994;15:435-444
Tice H, Barnes PD, Goumnerova L, Scott RM, Tarbell NJ. Pediatric and adolescent oligodendrogliomas. AJNR Am J Neuroradiol 1993;14:1293-1300
Smith AS, Wiznitzer M, Karaman BA, Horwitz SJ, Lanzieri CF. MRA detection of vascular occlusion in a child with progeria. AJNR Am J Neuroradiol 1993;14:441-443
Seidenwurm D, Berenstein A, A. H, Kowalski H. Vein of Galen malformation: correlation of clinical presentation, arteriography, and MR imaging. AJNR Am J Neuroradiol 1991;12:347-354
Horowitz MB, Jungreis CA, Quisling RG, Pollack I. Special report. Vein of Galen aneurysms: a review and current prospective. AJNR Am J Neuroradiol 1994;15:1486-1496
Banna M, Lasjaunias P. Intracavernous carotid aneurysm associated with proptosis in a 13-month-old girl. AJNR Am J Neuroradiol 1991;12:969-970
Heindel W, Kugel H, Roth B. Noninvasive detection of increased glycine content by proton MR spectroscopy in the brains of two infants with nonketotic hyperglycinemia. AJNR Am J Neurol 1993;14:629-636
Cortey A, Jarvik JG, Lenkinski RE, et al. Proton MR spectroscopy of brain abnormalities in neonates born to HIV-positive mothers. AJNR Am J Neuroradiol 1994;15:1853-1860
Nomura Y, Sakuma H, Takeda K, Tagami T, Okuda Y, Nakagawa T. Diffusional anisotrophy of the human brain associated with diffusion-weighted MR: relation with normal brain development and aging. AJNR Am J Neuroradiol 1994;15:231-238
Hill CAR, Gibson PJ. Ultrasound determination of the normal location of the conus medullaris in neonates. AJNR Am J Neuroradiol 1995;16:469-478
Barr LL, McCullough PJ, Ball WS, Krasner BH, Garra BS, Deddens JA. Quantitative sonographic feature analysis of clinical infant hypoxia: a pilot study. AJNR Am J Neuroradiol 1996;17:1025-1032
Belden CJ, Mancuso AA, Kotzur IM. The developing anterior skull base: CT appearance from birth to 2 years of age. AJNR Am J Neuroradiol 1997;18:811-818
Hudgins PA, Siegel J, Jacobs I, Abramowsky CR. The normal pediatric larynx on CT and MR. AJNR Am J Neuroradiol 1997;18:239-246
Norton KI, Som PM, Shugar JMA, Rothchild MA, Popper L. Subcutaneous fat necrosis of the newborn: CT findings of head and neck involvement. AJNR Am J Neuroradiol 1997;18:547-550
Garant M, Oudjhane K, Sinsky A, O'Gorman AM. Duplicated odontoid process: plain radiographic and CT appearance of a rare congenital anomaly of the cervical spine. AJNR Am J Neuroradiol 1997;18:1719-1720
Robertson RA, Maier SE, Robson CD, Mulkern RV, Karas PM, Barnes PD. MR line-scan diffusion imaging of the brain in children. AJNR Am J Neuroradiol 1999;20:419-426
Castillo M, Green L, Kwock Leal. Proton MR spectroscopy in patients with neurofibromatosis type 1: evaluation of hamartomas and clinical correlation. AJNR Am J Neuroradiol 1995;16:141-148
Shepherd CW, Houser OW, Gomez MR. MR findings in tuberous sclerosis complex and correlation with seizure development and mental impairment. AJNR Am J Neuroradiol 1995;16:149-224
Castillo M, Kwock L, Green C. MELAS syndrome: imaging and proton MR spectroscopic findings. AJNR Am J Neuroradiol 1995;16:233-240
Castellote A, Vera J, Vasquez E, Roig M, Belmonte JA, Rovira A. MR in adrenoleukodystrophy: atypical presentation as bilateral frontal demyelination. AJNR Am J Neuroradiol 1995;16:814-815
Kim TS, Kim IO, Kim WS, et al. MR of childhood metachromatic leukodystrophy. AJNR Am J Neuroradiol 1997;18:733-738
Takanashi J, Sugita K, Osaka H, Ishii M, Niimi H. Proton MR spectroscopy in Pelizaeus-Merzbacher disease. AJNR Am J Neuroradiol 1997;18:533-535
Cure’ JK, Holden KR, Van Tassel P. Progressive venous occlusion in a neonate with Sturge-Weber syndrome: demonstration with MR venography. AJNR Am J Neuroradiol 1995;16:1539-1542
Terada H, Barkovich AJ, Edwards MSB, Ciricillo SF. Evolution of high-intensity basal ganglia lesions on T-weighted MR in neurofibromatosis type 1. AJNR Am J Neuroradiol 1996;17:755-804
Rajanayagam V, Grad J, Krivit Weal. Proton MR spectroscopy of childhood adrenoleukodystrophy. AJNR Am J Neuroradiol 1996;17:1013-1024
Rajanayagam V, Balthazor M, Shapiro EG, Krivit W, Lockman L, Stillman AE. Proton MR spectroscopy and neuropsychological testing in adrenoleukodystrophy. AJNR Am J Neuroradiol 1997;18:1909-1914
Barkovich AJ, Rowley HA, Andermann F. MR in partial epilepsy: value of high-resolution volumetric techniques. AJNR Am J Neuroradiol 1995;16:339-344
Lehericy S, Dormont D, Semah F, et al. Developmental abnormalities of the medial temporal lobe in patients with temporal lobe epilepsy. AJNR Am J Neuroradiol 1995;16:617-626
Takanashi J, Sugita K, Fujii K, Niimi H. MR Evaluation of tuberous sclerosis: increased sensitivity with fluid-attenuated inversion recovery and relation to severity of seizures and mental retardation. AJNR Am J Neuroradiol 1995;16:1923-1935
Ozawa H, Sasaki M, Sugai Keal. Single-photon emission CT and MR findings in Kluver-Bucy syndrome and Reye syndrome. AJNR Am J Neuroradiol 1997;18:540-542
Bronen RA, Vives KP, Kim JH, Fulbright RK, Spencer SS, Spencer DD. Focal cortical dysplasia of taylor, balloon cell subtype: MR differentiation from low-grade tumors. AJNR Am J Neuroradiol 1997;18:1141-1152
Ho SS, Kuzniecky RI, Gilliam F, Faught E, Bebin M, Morawetz R. Congenital porencephaly: MR features and relationship to hippocampal sclerosis. AJNR Am J Neuroradiol 1998;19:135-135
Barkovich AJ, Rowley H, Bollen A. Correlation of prenatal events with the development of polymicrogyria. AJNR Am J Neuroradiol 1995;16:882-827
Sankar R, Curran JG, Kevill JW, Rintahaka PJ, Shewmon DA, Vinters HV. Microscopic cortical dysplasia in infantile spasms: evolution of white matter abnormalities. AJNR Am J Neuroradiol 1995;16:1265-1272
Dietrich RB, Lis LE, Greensite FS, Pitt D. Normal MR appearance of the pituitary gland in the first 2 years of life. AJNR Am J Neuroradiol 1995;16:1413-1421
Chen CY, Zimmerman RA, Faro Seal. MR of the cerebral operculum: topographic identification and measurement of interopercular distances in healthy infants and children. AJNR Am J Neuroradiol 1995;16:1677-1688
Kier EL, Truwit CL. The normal and abnormal genu of the corpus callosum: an evolutionary, embryologic, anatomic and MR analysis. AJNR Am J Neuroradiol 1996;17:1631-1642
Kier EL, Kim JH, Fulbright RK, Bronen RA. Embryology of the human fetal hippocampus: MR imaging, anatomy, and histology. AJNR Am J Neuroradiol 1997;18:525-532
Steen RG, Ogg RJ, Reddick WE, Kingsley PB. Age-related changes in the pediatric brain: quantitative MR evidence of maturational changes during adolescence. AJNR Am J Neuroradiol 1997;18:819-828
Nakagawa H, Iwasaki S, Kichikawa Keal. Normal myelination of anatomic nerve fiber bundles: MR analysis. AJNR Am J Neuroradiol 1998;19:1129-1136
Brisse H, Fallet C, Sebag G, Nessmann C, Blot P, Hassan M. Supratentorial parenchyma in the developing fetal brain: in vitro MR study with histologic comparison. AJNR Am J Neuroradiol 1997;18:1491-1498
Biondi A, Nogeuira H, Dormont Deal. Are the brains of monozygotic twins similar? A three-dimensional MR study. AJNR Am J Neuroradiol 1988;19:1361-1367
Barkovich AJ. Neuroimaging manifestations and classification of congenital muscular dystrophies. AJNR Am J Neuroradiol 1998;19:1389-1396
Barkovich AJ, Westmark K, Partridge C, Sola A, Ferriero DM. Perinatal asphyxia: MR findings in the first 10 days. AJNR Am J Neuroradiol 1995;16:427-439
Barkovich AJ, Sargent SK. Profound asphyxia in the premature infant: imaging findings. AJNR Am J Neuroradiol 1995;16:1837-1846
Castillo M, Fordham LA. MR in neurologically symptomatic newborns after vacuum extraction delivery. AJNR Am J Neuroradiol 1995;16:816-817
Martich-Kriss V, Kollias SS, Ball WS. MR findings in kernicterus. AJNR Am J Neuroradiol 1995;16:819-821
Ghazi-Birry HS, Brown WR, Moody DR, Challa VR, Block SM, Reboussin DM. Human germinal matrix: venous origin of hemorrhage and vascular characteristics. AJNR Am J Neuroradiol 1997;18:219-230
Barkovich AJ, Ali FA, Rowley HA, Bass N. Imaging patterns of neonatal hypoglycemia. AJNR Am J Neuroradiol 1998;19:523-528
Barkovich AJ, Hajnal BL, Vigneron D, et al. Prediction of neuromotor outcome in perinatal asphyxia: evaluation of MR scoring systems. . AJNR Am J Neuroradiol 1998;19:143-150
Aida N, Nishimura G, Hachiya Y, Matsui K, Takeuchi M, Itani Y. MR imaging of perinatal brain damage: comparison of clinical outcome with initial follow-up MR findings. AJNR Am J Neuroradiol 1998;19:1909-1922

Main menu

User menu

Search

American Journal of Neuroradiology

The First 5 Years (1980–1984)

The Golden Age of Sonography and CT

The Next Five Years (1985–1989)

The Contribution of MR Takes Shape

The Decade of the Brain (1990–1995)

The Early Years

The Decade of the Brain (1995–1999)

Prelude to the Future

References

News and Updates

Resources

Opportunities

American Society of Neuroradiology