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Frequency and Prediction of Abnormal Findings on Neuroimaging of Infants with Bulging Anterior Fontanelles

Yi-Fang Tu, MD, Hung-Yi Chuang, MD, PhD, Chao-Ching Huang, MD, Chia-Chang Chuang, MD, Shih-Min Wang, MD, Ming-Che Tsai, MD, Chin-Hsien Chi, MD, Ming-Che Chuang, MD Abstract

Objectives: This study sought to determine the frequency of clinically significant abnormal findings on neuroimaging using neurosonography (NS) in infants with bulging anterior fontanelles (BAFs) and to identify infants at high or low risk for clinically significant abnormal findings on neuroimaging. Methods: NS was performed in 45 consecutive infants with BAFs brought to the emergency department of a tertiary care hospital. NS reports were categorized as normal, clinically insignificant abnormal, or clinically significant abnormal. For each patient, demographic data, laboratory test results, and clinical diagnosis and outcome were obtained for analysis. Results: Eighteen febrile and 27 nonfebrile infants with BAFs were evaluated. Clinically significant abnormal findings on NS were noted in 16 of 45 patients (36%), five of whom were febrile and 11 of whom were nonfebrile. Brain edema resulting from infection was the most common finding on NS. Univariate analysis indicated that age younger than two months in febrile patients and abnormal findings on neurologic examination in nonfebrile patients were significant clinical predictors for clinically significant abnormal findings on NS in infants with BAFs. Patients presenting with either of these clinical predictors were identified as high risk for abnormal findings on NS. Of the high-risk patients, 15 of 17 patients (88%) had clinically significant abnormal findings on NS, compared with one of 28 patients (4%) in the low-risk group. Conclusions: This study shows a 36% prevalence of clinically significant abnormal findings on NS in infants with BAFs. Emergent neuroimaging should be considered for infants who meet high-risk criteria: 1) febrile children younger than two months or 2) nonfebrile children with abnormal findings on neurologic examination. Key words: bulging anterior fontanelle; infant; neurosonography; neuroimaging. ACADEMIC EMERGENCY MEDICINE 2005; 12:1185­1190.

The infant's anterior fontanelle offers the physician a window into the infant's developing brain and general state of health. A bulging anterior fontanelle (BAF) is often associated with increased intracranial pressure, which may indicate underlying neurologic or other systemic illness.1­8 The literature reports a variety of causes of BAFs that can be grouped into two major categories: 1) intracranial space-occupying lesions or structural damage and 2) systemic illness.1­8 An unknown fraction of these cases may require immediate intervention, such as cases of intracranial space-occupying lesions or structural damage. Quantifiable clinical data regarding these cases are needed to determine the need for

From the Departments of Emergency Medicine (Y-FT, C-CC, S-MW, M-CT, C-HC, M-CC) and Pediatrics (C-CH), National Cheng Kung University Hospital, Tainan, Taiwan; and Department of Clinical Research, Kaohsiung Medical University Hospital (H-YC), Kaohsiung, Taiwan. Received October 31, 2004; revisions received March 21, 2005, and May 10, 2005; accepted May 11, 2005. Address for correspondence and reprints: Yi-Fang Tu, MD, Department of Emergency Medicine, National Cheng Kung University Hospital, 138, Sheng-Li Road, Tainan 704, Taiwan. Fax: 886-6-235-9562; e-mail: [email protected] doi:10.1197/j.aem.2005.05.038

neuroimaging in infants with BAFs. To our knowledge, however, no prior study has determined the frequency of intracranial lesions or delineated the use of neuroimaging in infants with BAFs. Among the modalities available for neuroimaging in infants, neurosonography (NS) has the advantage of portability, availability, low cost, and nonirradiation.9­11 As an additional advantage, infants need not be sedated during NS. These advantages make NS a likely candidate for screening for intracranial lesions in infants with BAFs. Hence, to assess the yield of routine NS in infants with BAFs presenting to an emergency department (ED), we undertook this study to collect prospective data on historical features, physical and neurologic findings, and NS results. Our aim was to determine the frequency of clinically significant intracranial abnormalities using NS in infants with BAFs and to identify infants at high or low risk for clinically significant abnormal pathology detected by neuroimaging.

METHODS

Study Design. This was a prospective consecutive case series performed in an urban, university-affiliated pediatric ED with an annual census of approximately 10,400

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pediatric patient visits. The study was approved by our institutional review board. Written informed consent was obtained from the parents or caretakers for all participating patients. Study Setting and Population. The study took place between August 2002 and March 2004. A convenience sample of patients who presented to the ED with BAFs on physical examination, as identified by managing attending pediatric emergency physicians or senior pediatric residents, were eligible for enrollment. There were no age exclusions; all patients were accepted if the anterior fontanelle was open. BAF was defined as when palpation during physical examination revealed a tense or bulging fontanelle in patients who were quiet and in an upright position.12,13 Study Protocol. Complete historical and clinical data, including findings on physical examination, were collected on all study patients. Laboratory tests were performed at the discretion of the managing attending pediatric emergency physicians or senior pediatric residents. Patients with a tympanic temperature $38°C were designated as febrile. Septic workup was performed for all febrile infants (n ¼ 18) according to their clinical symptoms and results of their physical examination. Cerebrospinal fluid examination was also suggested to the parents of all febrile infants as a part of the workup; the parents of only one patient refused the lumbar puncture, but this patient was not excluded from our study. Neurologic examination of all study patients was performed by a pediatric neurologist (Y-FT), who provided on-call coverage 24 hours per day, 365 days per year during the study period. The examination included assessment of 1) mental status; 2) status of gross and fine motor functions, including developmental status, muscle power, muscle tone, and reflexes; 3) social behavior such as social smiling, pointing, and social body language (e.g., head nodding for thanks or yes); and 4) sensory screening such as orientation reflex for screening the audition and pain response for identifying peripheral sensation. All examinations were adjusted for individual ages.1,9,12 NS was then performed by pediatric sonographers with a group average of nine years of experience in the field of NS. The NS reading was performed immediately by the pediatric neurologist (Y-FT). Patients were then discharged or admitted according to the clinical condition and NS findings. Measurements. All study patients underwent an NS examination via a real-time ultrasound imaging unit (model SSD-663; Aloka, Tokyo, Japan) equipped with 5.0- and 7.5-MHz sector transducers. The examinations were performed through the anterior and/or lateral fontanelle.14­16 All images were reviewed blindly and categorized by the same reader (a pediatric neurologist

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[C-CH]) for the final analysis.16 Imaging reports were categorized as normal, clinically insignificant abnormal, and clinically significant abnormal. NS findings such as lenticulostriate vasculopathy and mild to moderate extracerebral fluid collections were regarded as clinically insignificant abnormal NS.17 Clinically significant abnormal neuroimaging results were those that resulted in a change in the patient's management (e.g., edema, hemorrhage, or tumor) or prognosis (e.g., congenital malformation).18 For all study subjects, the need for intervention in the ED or during subsequent hospital admission was determined from a review of the medical records. Patients discharged from the ED were all contacted by telephone two weeks after discharge to ensure the final diagnosis. Admitted patients were followed up to final surgical or clinical diagnosis. Neurologic outcome was also recorded on discharge or at the follow-up outpatient department visit by pediatric neurologists (Y-FT, C-CH). Any impairment of motor status, delay of developmental milestone, or presence of epilepsy was regarded as having neurologic sequela. Data Analysis. Statistical analysis was conducted using SPSS version 10 (SPSS Inc., Chicago, IL). Parametric data were expressed as the mean 6 standard deviation (SD). Chi-square tests (Fisher's exact test) were used for categorical variables and Student's t-test for continuous variables to test significant differences between the febrile and nonfebrile groups. Odds ratios and Fisher's exact test were calculated for univariate analysis of the relationships between dichotomous clinical predictor variables, such as age younger than two months, gender, symptoms other than a BAF, abnormal findings on neurologic examination, and clinically significant abnormal findings on NS. Throughout the study, a p-value of , 0.05 was considered statistically significant, and all probabilities were two tailed. Results of comparisons are presented with 95% confidence intervals.

RESULTS

Clinical Features. A total of 17,312 patients visited the pediatric ED during the 20-month study period. Forty-five patients (0.3%; 20 boys and 25 girls) with BAFs were enrolled in our study. The mean (6SD) age of the study patients was 4 (63.3) months (range, 2 days to 16 months). Neurologic examination showed abnormal findings in 15 of 45 patients (33%). Global hypotonia was the most common presentation, followed by altered mental status and loss of upward gaze (sunset eye sign). Eighteen patients exhibited fever, and 27 patients did not. The clinical characteristics in the febrile and nonfebrile groups are shown in Table 1.

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abnormal findings on NS were present in 16 of 45 patients (36%), five in the febrile group and 11 in the nonfebrile group. There was no significant difference in the prevalence of clinically significant abnormal findings on NS between the febrile and nonfebrile groups (Table 1). The 16 patients with clinically significant abnormal findings on NS are categorized in Table 3. Brain edema (n ¼ 5) and hydrocephalus (n ¼ 4) accounted for 56% of the abnormalities. Three of the five patients with brain edema had a CNS infection, including two with group B streptococcal meningoencephalitis and one with aseptic meningitis. One patient with edema had metabolic encephalopathy with a deficiency of ornithine transcarbamylase, and one case with edema resulted from shaken baby syndrome. The other patient with shaken baby syndrome had a massive subdural effusion on NS. In total, two patients underwent follow-up computed tomographic (CT) scans and nine underwent magnetic resonance imaging. All the follow-up neuroimaging findings correlated with the NS results. Prediction of Clinically Significant Abnormal Findings on NS. Two clinical variables in univariate analyses had significant association with clinically significant abnormal findings on NS in the febrile group: 1) age of onset younger than two months and 2) an abnormal finding on neurologic examination. The latter also correlated significantly with clinically

TABLE 1. Clinical Characteristics in 45 Patients with Bulging Anterior Fontanelles

Febrile Patients No. Gender (male/female) Age of onset (mo) No. (%) with abnormal findings on neurologic examination Findings on NS, no. (%) Abnormal Clinically significant abnormal Outcome, no. (%) Neurologic sequela Death NS ¼ neurosonography. 18 8/10 4.06 6 2.64 Nonfebrile Patients 27 12/15 3.94 6 3.74 p-value

0.911

3 (17) 5 (28) 5 (28) 2 (11) 1 (6)

12 (44) 18 (67) 11 (41) 9 (33) 4 (15)

0.063 0.016 0.527 0.079 0.634

Final clinical diagnosis is presented in Table 2. The most common etiology of BAFs in our study was infection, primarily involving the central nervous system (CNS) (n ¼ 9), followed by CNS malformation. Five of the nine patients with CNS infection had viral CNS infections, three of which were confirmed as enterovirus. Among the patients with respiratory tract infection, the common pathogens were adenovirus and influenza virus. Neurosonography. Abnormal NS results were obtained for 23 of 45 patients (51%). Clinically significant

TABLE 2. Clinical Diagnosis, Abnormal Findings on Neurologic Examination, and Clinically Significant Abnormal Findings on Neurosonography in 45 Patients with Bulging Anterior Fontanelles

Febrile Patients, n Clinical Diagnosis Infection CNS Aseptic meningitis GBS meningoencephalitis Neurotuberculosis Respiratory tract infection Upper respiratory tract Lower respiratory tract Roseola infantum CNS malformation Ventriculomegaly Hydrencephaly Agenesis of septum pellucidum Stenosis of aqueduct of Sylvian Extracerebral fluid collection Neoplasm Medulloblastoma Papilloma Shaken baby syndrome Intracranial hemorrhage Metabolic encephalopathy Ornithine transcarbamylase deficiency Unidentified aNE 3 -- 3 -- -- -- -- 0 csaNS 4 1 3 -- -- -- -- 0 Total 15 4 3 -- 4 2 2 0 aNE 1 -- -- 1 -- -- -- 3 1 1 1 -- 0 3 2 1 2 1 1 1 Nonfebrile Patients, n csaNS 1 -- -- 1 -- -- -- 3 -- 1 1 1 0 3 2 1 2 1 1 0 Total 4 1 -- 1 2 -- -- 6 3 1 1 1 4 3 2 1 2 1 1 6 Total, N (%) 19 (42) 5 3 1 6 2 2 6 (13) 3 1 1 1 4 (9) 3 (7) 2 1 2 (4) 2 (4) 1 (2) 8 (18)

0 0

0 0

0 0

0 0 0 0

0 1 0 0

0 1 0 2

aNE ¼ abnormal findings on neurologic examination; csaNS ¼ clinically significant abnormal findings on neurosonography; CNS ¼ central nervous system; GBS ¼ group B streptococcus.

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TABLE 3. Clinically Significant Abnormal Findings on Neurosonography in 16 Patients

Significant Neurosonographic Abnormality Brain edema Hydrocephalus with neoplasm (3) or aqueduct stenosis (1) Central nervous system malformation Hydroencephaly (1) Agenesis of septum pellucidum (1) Intracranial hemorrhage Intraventricular hemorrhage with venous infarction (1) Subdural hemorrhage with transtentorial herniation (1) Massive subdural effusion Subarachnoid exudate Neurotuberculosis No. of Patients (%) 5 (31) 4 (25) 2 (13)

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had no sequela at the mean age of 14 months (range, 3­22 months) at follow-up. Among the eight patients with neurologic sequela, four had global developmental delay, three had impairment of motor status, and two had epilepsy. Of the patients without clinically significant abnormal findings on NS, none needed emergent medical intervention in the ED but three showed developmental delay at follow-up.

2 (13)

DISCUSSION

1 (6) 1 (6) 1 (6)

significant abnormal findings on NS in the nonfebrile group (Table 4). According to these two clinical predictors, the study infants with BAFs were repartitioned into high- and low-risk groups for clinically significant abnormal findings on NS (Figure 1). Fifteen of 17 patients (88%) in the high-risk group had clinically significant abnormal findings on NS compared with one of 28 patients (4%) in the low-risk group. The only patient who was classified as low risk who had clinically significant abnormal findings on NS was a 2-day-old baby. He was brought to the ED because of poor feeding after birth but did not have a fever. Routine neurologic examination showed no abnormality other than a BAF, but emergent NS showed hydrocephalus with aqueduct stenosis. The sensitivity for clinically significant abnormal findings on NS in the high-risk group was 93.6%, and the specificity was 93.1%. The negative predictive value was 96.4%. Clinical Outcome. Of the 16 patients with clinically significant abnormal findings on NS, 13 patients (81%) needed emergent surgical (n ¼ 4) or medical (n ¼ 9) intervention. Five patients died, and eight patients had neurologic sequela. The remaining three patients

A BAF is considered a medical emergency because of its possible association with serious underlying CNS disease.19 Even though meningitis should be ruled out first, other pathologic causes, such as space-occupying lesions, hydrocephalus, or intracranial hemorrhage, must be considered as well.19 For infants coming to the ED with BAFs, the role of emergent neuroimaging is not well defined, and the prevalence of neuroimaging abnormalities in this infant population has not been identified in the literature. Our study using NS as a tool of emergent neuroimaging shows a 36% prevalence of clinically significant abnormal findings on NS in infants with BAFs, especially in febrile patients younger than two months and in nonfebrile patients with abnormal findings on neurologic examination. The clinical causes of BAFs are represented by a broad range of diagnoses, as described in the literature and in our study.2­8 Our most common clinical diagnosis was infection, primarily involving the CNS. Approximately two thirds of our infection cases were the result of viral pathogens such as enterovirus, human herpesvirus-6, adenovirus, and influenza virus. All patients except one (14 of 15 [93%]) recovered without sequela. One third of our infection cases were bacterial, all of which were CNS infections. All but one bacterial case (3 of 4 [75%]) had neurologic sequela at follow-up. In the literature, endocrine disorders (e.g., hyperthyroidism/hypothyroidism, pseudohypoparathyroidism, Addison's disease) and miscellaneous causes (e.g., hypervitaminosis A, lead toxicity, and aluminum toxicity) can also induce BAFs.1­3,8 These causes were not found in our series.

TABLE 4. Univariate Analysis of Clinical Variables for Infants with Clinically Significant Abnormal Findings on Neurosonography in Febrile and Nonfebrile Groups

Febrile Clinical Variable Demographic data Age younger than two months Gender Male Female Symptoms other than bulging anterior fontanelle Abnormal findings on neurologic examination OR (95% CI) Infinity 2.4 (0.3, 19.8) 0.42 (0.05, 3.5) 9 (0.9, 108.3) Infinity p-value ,0.001 0.608 Nonfebrile OR (95% CI) 1.71 (0.3, 9.1) 3.85 0.26 3.85 70 (0.8, 19.5) (0.05, 1.3) (0.8, 19.5) (5.6, 882.2) p-value 0.675 0.130

0.118 0.012

0.130 ,0.001

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Figure 1. Forty-five patients with bulging anterior fontanelles were categorized into high- or low-risk groups for clinically significant abnormal findings on neurosonography by clinical predictors. BAF ¼ bulging anterior fontanelle; NE ¼ neurologic examination; pts ¼ patients.

A BAF may be the result of any underlying pathophysiologic mechanism that produces increased intracranial pressure (e.g., brain parenchyma expansion, ventricular enlargement, subdural or subarachnoid space change, increased intravascular or cerebral spinal fluid volume, and so on).19,20 In our patients, brain parenchyma expansion caused by brain edema, mainly resulting from CNS infection, accounted for the most common finding on NS. Ventricular enlargement caused by hydrocephalus and ventriculomegaly followed. One patient with a BAF, categorized in the CNS malformation group, had agenesis of the septum pellucidum. Agenesis of septum pellucidum itself could not explain the presentation of a BAF unless it was associated with other abnormalities. Barkovich et al.21 said that agenesis of the septum pellucidum is never seen as an isolated finding and is associated with a congenital brain malformation. The later magnetic resonance imaging study of this patient, obtained at one year of age, showed only mild ventriculomegaly associated with agenesis of the septum pellucidum. Because agenesis of the septum pellucidum has not been mentioned as a cause of BAFs in the literature,1­8 the BAF observed in this patient might result from an undetected associated abnormality; alternately, the agenesis of the septum pellucidum may be an incidental finding. Our repartition analysis, which was developed with the goal of having high sensitivity and clinical applicability (Figure 1), identified two criteria associated with a high risk for clinically significant abnormal findings on neuroimaging: 1) age younger than two months in febrile patients and 2) abnormal findings on neurologic examination in nonfebrile patients. According to the repartition, the sensitivity for clinically significant abnormal findings on neuroimaging in a high-risk group could be as high as 93.6%. Our single exception is the nonfebrile patient who had normal findings on neurologic examination but who also had clinically significant abnormal findings

on NS. This patient was a two-day-old baby with hydrocephalus with aqueduct stenosis. He was born uneventfully but was brought to our ED because of poor feeding after birth. Routine neurologic examination showed no abnormality aside from a BAF. This patient exemplifies the fact that decreasing infant age correlates with increasing difficulty in obtaining reliable results from conventional neurologic examination. Nevertheless, neurologic examination should still be emphasized, and more attention should be paid to newborns with BAFs. To the best of our knowledge, there is no definite recommendation published to assist in managing patients with BAFs.1­8,19,20 In practice, a physician is likely to do a lumbar puncture, perhaps without any imaging study, in febrile patients with BAFs. In addition, any patients with a BAF and abnormal findings on neurologic examination would likely undergo a neuroimaging study to identify intracranial spaceoccupying lesions or structural damage. These practice patterns are similar to our criteria of high risk for clinically significant abnormal findings on neuroimaging. The new finding we have identified is that age younger than two months in febrile patients is also associated with a high risk for clinically significant abnormal findings on neuroimaging. Of our five febrile patients with clinically significant abnormal findings on NS, three showed brain edema, one demonstrated subarachnoid exudate, and the last had an intraventricular hemorrhage (idiopathic). The knowledge of brain edema and intraventricular hemorrhage had an impact on decision making regarding the performance of a lumbar puncture. For the patient with known subarachnoid exudates, the course of antibiotic therapy should be extended to four weeks. The role of neuroimaging in this type of high-risk patient is essential in clinical management. Many neuroimaging modalities may be used for evaluation of BAFs in infants. They include NS, CT

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scan, and magnetic resonance imaging.9 Although a CT scan is more readily available in the ED setting, NS is a more portable and nonirradiative neuroimaging modality for infants. As an additional advantage, infants need not be sedated during NS. Based on our findings, we encourage consideration of urgent neuroimaging for high-risk infants, but the choice of neuroimaging modality should be based on availability at different hospitals.

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LIMITATIONS

Because our ED was at a tertiary care hospital, the high frequency of abnormal findings on NS in patients with BAFs might not represent the incidence in the general population. Further, the number of patients with BAFs in our study was small, and other modalities of neuroimaging, such as CT scans or magnetic resonance imaging, were not available to all patients. It would be desirable to validate our clinical predictors on a larger patient population.

CONCLUSIONS

Our study shows a 36% prevalence of clinically significant abnormal findings on NS in infants with BAFs. In general, CNS infection should be ruled out first in patients with BAFs, especially those who are febrile. Emergent neuroimaging should be considered, based on our findings, in infants with BAFs who meet high-risk criteria for clinically significant abnormal findings on neuroimaging: 1) febrile and younger than two months and 2) nonfebrile with abnormal findings on neurologic examination. These predictors might be useful if the emergency physician wants to limit neuroimaging to patients at high risk for intracranial abnormalities. References

1. Stoll BJ, Kliegman RM. The newborn infant. In: Behrman RE, Kliegman RM, Jenson HB (eds). Textbook of Pediatrics, ed 17. Philadelphia, PA: Saunders, 2003, pp 523­31. 2. Green M. The head. In: Green M (ed). Pediatric Diagnosis: Interpretation of Symptoms and Signs in Children and Adolescents, ed 6. Philadelphia, PA: Saunders, 1990, p 9.

3. Kiesler J, Ricer R. The abnormal fontanel. Am Fam Physician. 2003; 67:2547­52. 4. Kimberlin DW. Meningitis in the neonate. Curr Treat Options Neurol. 2002; 4:239­48. 5. Biswas AC, Molla MA, Al-Moslem K. A baby with bulging anterior fontanelle [case report]. Lancet. 2000; 356:132. 6. Tamer SK, Tamer U, Warey P. Infantile pseudotumor cerebri related to viral illness. Indian J Pediatr. 1996; 63:645­9. 7. Chaturvedi P, Bannerjee KS, Gawdi A. Bulging anterior fontanel after DPT vaccination. Indian J Pediatr. 1994; 61:111­2. 8. Bass MH, Fisch GR. Increased intracranial pressure with bulging fontanel. A symptom of vitamin A deficiency in infants. Neurology. 1961; 11:1091­4. 9. Volpe JJ. Specialized studies in the neurological evaluation. In: Volpe JJ (ed). Neurology of the Newborn, ed 4. Philadelphia, PA: Saunders, 2000, pp 134­77. 10. Huang CC, Chen CY, Yang HB, Wang SM, Chang YC, Liu CC. Central nervous system candidiasis in very low-birth-weight premature neonates and infants: US characteristics and histopathologic and MR imaging correlates in five patients. Radiology. 1998; 209:49­56. 11. Barkovich AJ. The encephalopathic neonate: choosing the proper imaging technique. Am J Neuroradiol. 1997; 18:1816­20. 12. Taeusch HW, Sniderman S. Initial evaluation: history and physical examination of the newborn. In: Taeusch HW, Ballard RA (eds). Avery's Diseases of the Newborn, ed 7. Philadelphia, PA: Saunders, 1998, pp 334­53. 13. Fletcher MA. Head and neck region. In: Fletcher MA (ed). Physical Diagnosis in Neonatology. Philadelphia, PA: Lippincott-Raven, 1998, pp 173­235. 14. Barr LL. Neonatal cranial ultrasound. Radiol Clin North Am. 1999; 37:1127­46. 15. Pigadas A, Thompson JR, Grube GL. Normal infant brain anatomy: correlated real-time sonograms and brain specimens. Am J Roentgenol. 1981; 137:815­20. 16. Govaert P, de Vries LS (eds). An Atlas of Neonatal Brain Sonography. London, England: Mac Keith Press, 1997. 17. Chen CY, Chou TY, Zimmerman RA, Lee CC, Chen FH, Faro SH. Pericerebral fluid collection: differentiation of enlarged subarachnoid spaces form subdural collections with color Doppler US. Radiology. 1996; 201:389­92. 18. Sharma S, Riviello JJ, Harper MB, Baskin MN. The role of emergent neuroimaging in children with new-onset afebrile seizures. Pediatrics. 2003; 111:1­5. 19. Simon MW, Simon NP. Bulging anterior fontanel [letter]. Arch Pediatr Adolesc Med. 1998; 152:608. 20. Rothman SM, Lee BC. What bulges under a bulging fontanel? Arch Pediatr Adolesc Med. 1998; 152:100­1. 21. Barkovich AJ, Norman D. Absence of the septum pellucidum: a useful sign in the diagnosis of congenital brain malformations. Am J Roentgenol. 1989; 152:353­60.

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