Department of Neurosurgery, Emory University; and 2 Pediatric Neurosurgery Associates at Children s Healthcare of Atlanta, Georgia
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1 J Neurosurg Pediatrics 14: , 2014 AANS, 2014 Poor correlation between head circumference and cranial ultrasound findings in premature infants with intraventricular hemorrhage Clinical article Martha-Conley E. Ingram, B.S., 1 Anna L. Huguenard, B.S., B.A., 1 Brandon A. Miller, M.D., Ph.D., 1 and Joshua J. Chern, M.D., Ph.D. 2 1 Department of Neurosurgery, Emory University; and 2 Pediatric Neurosurgery Associates at Children s Healthcare of Atlanta, Georgia Object. Intraventricular hemorrhage (IVH) is the most common cause of hydrocephalus in the pediatric population and is particularly common in preterm infants. The decision to place a ventriculoperitoneal shunt or ventricular access device is based on physical examination findings and radiographic imaging. The authors undertook this study to determine if head circumference (HC) measurements correlated with the Evans ratio (ER) and if changes in ventricular size could be detected by HC measurements. Methods. All cranial ultrasound (CUS) reports at the authors institution between 2008 and 2011 were queried for terms related to hydrocephalus and IVH, from which a patient cohort was determined. A review of radiology reports, HC measurements, operative interventions, and significant clinical events was performed for each patient in the study. Additional radiographic measurements, such as an ER, were calculated by the authors. Significance was set at a statistical threshold of p < 0.05 for this study. Results. One hundred forty-four patients were studied, of which 45 (31%) underwent CSF diversion. The mean gestational age and birth weight did not differ between patients who did and those who did not undergo CSF diversion. The CSF diversion procedures were reserved almost entirely for patients with IVH categorized as Grade III or IV. Both initial ER and HC were significantly larger for patients who underwent CSF diversion. The average ER and HC at presentation were 0.59 and 28.2 cm, respectively, for patients undergoing CSF diversion, and 0.34 and 25.2 cm for those who did not undergo CSF diversion. There was poor correlation between ER and HC measurements regardless of gestational age (r = 0.13). Additionally, increasing HC was not found to correlate with increasing ERs on consecutive CUSs (φ = -0.01, p = 0.90). Patients who underwent CSF diversion after being followed with multiple CUSs (10 of 45 patients) presented with smaller ERs and HC than those who underwent CSF diversion after a single CUS. Just prior to CSF diversion surgery, the patients who received multiple CUSs had ERs, but not HC measurements, that were similar to those in patients who underwent CSF diversion after a single CUS. Conclusions. The HC measurement does not correlate with the ER or with changes in ER and therefore does not appear to be an adequate surrogate for serial CUSs. In patients who are followed for longer periods of time before CSF shunting procedures, the ER may play a larger role in the decision to proceed with surgery. Clinicians should be aware that the ER and HC are not surrogates for one another and may reflect different pathological processes. Future studies that take into account other physical examination findings and long-term clinical outcomes will aid in developing standardized protocols for evaluating preterm infants for ventriculoperitoneal shunt or ventricular access device placement. ( Key Words intraventricular hemorrhage hydrocephalus cranial ultrasound head circumference prematurity Intraventricular hemorrhage (IVH) is the most common cause of hydrocephalus in the pediatric population. It is estimated that approximately 30% 59% of all live-born, preterm infants will develop IVH and that 36% of all extremely premature infants (gestational age Abbreviations used in this paper: CUS = cranial ultrasound; ER = Evans ratio; HC = head circumference; ICP = intracranial pressure; IVH = intraventricular hemorrhage; VAD = ventricular access device; VPS = ventriculoperitoneal shunt. < 25 weeks) will develop severe hemorrhage classified as Grade III or IV. 6,13 The long-term sequelae of IVH include parenchymal injury, hydrocephalus, cerebral palsy, and cognitive delay. 1,16,17 Currently, there is no consensus regarding the indications for, or the timing of, the treatment of hydrocephalus following IVH in premature infants. Clinical suspicion for IVH can be raised through assessment of several factors including apneic or bradycardic episodes, a bulging anterior fontanelle, and increased head circumference (HC), and is confirmed by findings 184 J Neurosurg: Pediatrics / Volume 14 / August 2014
2 Head circumference and ultrasound findings on cranial ultrasound (CUS). The presence of an apneic or bradycardic episode suggests that hemorrhage is already severe and strongly predicts placement of a temporizing device or shunt. 13 Studies have demonstrated a positive correlation between findings on palpation of the anterior fontanelle and intracranial pressure (ICP). 9,15 The reliability of this physical examination finding has been verified, with an acceptable interrater reliability in evaluating the anterior fontanelle. 18 Nevertheless, guidelines for how these assessments can be used in clinical practice have not yet been established. Measuring HC at regular intervals in this population has long been thought to be an objective way to assess progression of hydrocephalus. However, the criterion of a 2 cm/week increase in HC as an indicator of posthemorrhagic hydrocephalus has been shown to be unreliable. 13 Using serial CUSs has become standard practice for many pediatric neurosurgeons to evaluate the need for shunt placement, although there is no evidence-based rationale for this practice. 4,14 Current practice is for physicians to use physical examination and radiographic findings without evidence of which factors are most predictive of a need for shunt placement. There is also no clear understanding of how well clinical and radiographic findings correlate in preterm infants. This study was undertaken to establish the correlation, or lack thereof, between HC and CUS findings, and to determine which of these clinical factors are most predictive for CSF diversion. Methods Patient Selection Institutional review board permission was obtained for this study. We queried our electronic medical record for CUS reports entered between 2008 and 2011 and containing the phrases intracranial hemorrhage, intraventricular hemorrhage, germinal matrix, bleed, or IVH. Patients with concurrent diagnosis of congenital malformations or hydrocephalus due to causes other than IVH were excluded. Patients born of term pregnancy (> 38 weeks) were excluded. A retrospective chart review was then conducted to collect data on the 144 patients identified. The following information was collected for each patient: gestational age at birth; birth weight; HC measurements; characteristics of each ultrasound performed, including the time interval between the scans; grade of IVH; presence and progression of associated hydrocephalus; and Evans ratio (ER). Other forms of imaging, including CT scans and MRI, were not included for analysis because the number of patients receiving imaging by these modalities was small. Additional clinical information was analyzed, including the date of placement of a VAD or shunt, the age at which diversion occurred, any revisions of shunts or shunt infections, and the date and cause of death of the patient where available. Ultrasound Imaging The authors evaluated all CUS images and reports. Grading of IVH followed the scale defined by Papile et al. 12 Children who presented to our facility with a history J Neurosurg: Pediatrics / Volume 14 / August 2014 of hemorrhage and documented posthemorrhagic hydrocephalus, but in whom no IVH was present on CUS imaging obtained at our institution, were labeled as having resolved hemorrhage but were still included in the study. If periventricular leukomalacia and cystic brain parenchymal changes followed a diagnosis of Grade IV hemorrhage, the patient was considered to continue carrying a Grade IV classification for analysis. The label of hydrocephalus was applied if the radiographic dictation included the terms hydrocephalus, ventriculomegaly, ventricular dilatation, or enlarged ventricles. We measured the ER, the ratio of the bifrontal horn diameter to the biparietal bone diameter, for each CUS scan. 7,10 Statistical Analysis Potential predictors of CSF diversion were analyzed, including initial birth weight, gestational age, presence of hydrocephalus on the initial CUS, interval worsening of hydrocephalus between CUSs, and ER on each CUS. Data were analyzed using the Student t-test of means. For the analysis of differences in ER and HC by IVH grade, ANOVA, Student t-test, and correlation studies were used as indicated in the text. Interscan changes in ER and HC were calculated and compared using the Pearson chisquare test for association. Significance was set at p < 0.05 for all parts of this study. Results Initial ER and HC as Predictors of CSF Diversion Presenting patients demographic data, initial HC mea surements, and radiographic findings are shown in Ta ble 1, allowing comparison between patients who progressed to surgical CSF diversion (n = 45) and those who did not (n = 99). The vast majority of patients in the study who underwent CSF diversion did so after receiving only 1 CUS at our institution (35 of 45 patients, 78%). Birth weight and gestational age at birth did not differ between patients who underwent CSF diversion and those who did not. As shown in Table 1, there was a significant difference in initial ER for children who did and did not undergo CSF diversion. Overall, the average ER in the group undergoing diversion was 0.59, compared with 0.34 in the group not progressing to diversion (p < 0.001). When patients were stratified by hemorrhage severity, a larger initial ER was observed in patients needing CSF diversion for resolved, mild-moderate, and severe hemorrhage. As with the ER, the initial HC was significantly different between children who did and did not progress to CSF diversion (p < 0.001), but this difference became less reliable as patients were stratified by hemorrhage severity. For patients with Grade I or II hemorrhage, initial HC was not a significant predictor of diversion (p = 0.087); patients with CSF diversion who had resolved or severe (Grade III or IV) hemorrhage had initial HC measurements that were significantly larger, but by a relatively narrow margin (p = and 0.041, respectively). Correlation Between ER and HC We used a correlation analysis to determine if HC 185
3 M. C. E. Ingram et al. TABLE 1: Comparison between demographic data in patients receiving CSF diversion and those who underwent no surgical diversion* Quality on Presentation Surgical CSF Diversion No Yes p Value no. of patients GA in wks at birth 27.4 (4.5) 27.2 (3.0) 0.79 birth weight in g (784.3) (446.8) 0.45 GA in wks at initial assessment (24.5) (4.4) 0.48 hemorrhage category resolved 6 (6.1%) 5 (11.1%) 0.32 mild-moderate (Grade I or II) 54 (54.5%) 4 (8.9%) <0.001 severe (Grade III or IV) 39 (39.4%) 36 (80.0%) <0.001 initial ER overall 0.34 (0.08) 0.59 (0.12) <0.001 resolved hemorrhage 0.27 (0.07) 0.62 (0.11) <0.001 mild-moderate hemorrhage 0.31 (0.04) 0.59 (0.16) <0.001 severe hemorrhage 0.39 (0.09) 0.59 (0.12) <0.001 initial HC in cm overall 25.2 (4.4) 28.2 (3.5) <0.001 resolved hemorrhage 34.5 (3.0) 30.3 (2.2) mild-moderate hemorrhage 25.5 (4.3) 29.3 (1.8) severe hemorrhage 23.4 (2.7) 24.7 (2.7) * Key demographic data obtained for all patients, stratifying many categories by grade of hemorrhage (resolved; mild-moderate [Grade I or II]; severe [Grade III or IV]) to demonstrate factors significantly different between patients who later received surgical CSF diversion and those who did not. Unless otherwise indicated, the numbers in parentheses represent the SD. GA = gestational age. The p values were calculated with either a chi-square or Student t-test. Significant differences (p < 0.05) are in boldface. and ER correlated on initial scans for patients overall or if stratified by gestational age ( 30 or < 30 weeks) at the time of imaging (Fig. 1). Initial HC measurements were not available for 14 patients. Contrary to our hypothesis, there was a significant correlation between initial ER and HC only in patients who underwent the first CUS at less than 30 weeks gestational age, and no significant correlation between initial CUS and ER overall (Table 2). Correlation Between Changes in ER and HC A contingency analysis was used to test if increases in ER were accompanied by changes in HC. We examined all patients who received > 1 scan without undergoing CSF diversion, analyzing all intervals between scans. A significant change in ER was set at 0.2, because this was similar to the difference between initial ERs in patients who did and did not undergo CSF diversion (Table 1). We chose 1.5 cm as a meaningful change in HC, taken from the study by Müller and Urlesberger, which showed 1.5 cm to be a sensitive indicator of increasing hydrocephalus. 11 The contingency association was analyzed with the Pearson chi-square test, revealing no significant association between changes in ER and changes in HC (Table 3). Characteristics of Patients Undergoing Delayed Versus Immediate CSF Diversion To better understand the decision to proceed with CSF diversion in patients who are followed for longer periods before surgery, we compared patients who received multiple CUS images before CSF diversion to those who received only 1 CUS prior to CSF diversion (Table 4). In 10 (22%) of 45 patients, > 1 scan was obtained before undergoing CSF diversion. Patients in this late CSF diversion group received an average of 4 CUSs before undergoing CSF diversion. Gestational age at birth and birth weight were not significantly different between patients who underwent early versus late CSF diversion, nor was the presence of high-grade IVH. Additionally, gestational age at the time of CSF diversion was not significantly different between the 2 groups. Initial HC and ER were significantly smaller in patients who underwent delayed CSF diversion (p < 0.01 for each); however, ER did not differ significantly between groups just prior to diversion (p = 0.22). Head circumference remained slightly smaller in patients who underwent CSF diversion at a later time (p = 0.034). Discussion Predictors of CSF Diversion: ER Versus HC Management of infants with hydrocephalus from IVH has been the subject of controversy, because many infants with IVH may have spontaneous resolution of symptoms without shunt insertion. 5 However, early interventions such as lumbar puncture have been associated with lower 186 J Neurosurg: Pediatrics / Volume 14 / August 2014
4 Head circumference and ultrasound findings TABLE 3: Contingency association between interval changes in HC and ER on all scans taken prior to diversion in all patients* Contingency ΔER 0.2 ΔER < 0.2 Totals ΔHC ΔHC < totals * Contingency association in changes of HC and ER over the entire observation period prior to diversion; includes all patients in whom > 1 scan was performed. Significant absolute changes in HC or ER between any 2 sequential scans was defined as 1.5 cm in HC or 0.2 in ER (see text). Scans obtained after diversion were not included in this analysis. φ = 0.01; p = 0.90 according to the Fisher test. This contingency association is not significant. Fig. 1. Scatterplot showing ER and HC for all patients on initial scan, stratified by < 30 weeks and 30 weeks gestational age (GA). The corresponding correlation study results are shown in Table 2. There were 130 patients in this group; 14 patients did not have initial HC measurements and were not included. rates of ventricular shunting and improved outcomes after IVH; 17 therefore, it is intuitive that any treatment for preterm hydrocephalus should be carried out as expeditiously as possible. There is little consensus on the management of patients with neonatal IVH and hydrocephalus, with high variability in treatment between centers. 8 Our data demonstrate, as expected, that infants who receive CSF diversion tend to present with higher grades of hemorrhage initially and that both initial HC and initial ER are larger in patients who undergo CSF diversion. Correlation of ER With HC Contrary to our hypothesis, we found a correlation between HC and ER only in patients less than 30 weeks gestational age at first scan, but not in our population overall. We also found no correlation between ER and HC changes that were deemed clinically significant and likely to be reliably detected. These findings cast doubt on the utility of HC as a surrogate for expanding ventricular size as measured by ER or may reflect the inherent variability of the measurement itself. In either instance, this reveals reservations for the utility of following serial HC measurements to assess progressive hydrocephalus. To our knowledge, there is no study of interrater reliability of HC measurement, nor are there any data indicating how variable either HC or ER may be within the same patient when evaluated within short time periods, such as < 24 hours. Most importantly, there is no evidence regarding how either HC or ER correlates with ICP, which is thought to be the underlying cause of brain injury in preterm infants with IVH. Comparing these 2 measurements with actual ICP readings could help determine a gold standard for choosing patients who would be most likely to benefit from early CSF diversion, and could help surgeons avoid performing unnecessary procedures. Changes in ER and HC as Patients Progress Toward CSF Diversion The vast majority of patients in our study who underwent CSF diversion had a VPS or VAD placed after the first CUS performed at our institution. This indicates that the clinical decision to place a diverting device is typically made rapidly. When CSF diversion occurred after serial imaging studies, the ER, but not HC, was found to have caught up with the measurements present in those who had undergone diversion after 1 imaging study. This finding indicates that neurosurgeons may rely on imaging characteristics more than HC changes when following the progression of hydrocephalus and deciding to place a TABLE 2: Correlation between ER and HC at initial scan in all patients, with corresponding regression analysis* Group No. of Patients Pearson Coefficient of Correlation r (df = n 2) R 2 Regression Coefficient M (slope) Intercept p Value overall 130 r (128) = <30 wks GA at initial scan 69 r (67) = wks GA at initial scan 61 r (59) = * Correlation between initial HC and ER in all patients prior to diversion, stratified by age as shown in Fig. 1. Correlation was significant (p < 0.05; boldface) only for the subgroup of patients < 30 weeks old at initial scan, but not for patients 30 weeks old or overall. Fourteen patients did not have an HC measured at initial scan. J Neurosurg: Pediatrics / Volume 14 / August
5 M. C. E. Ingram et al. TABLE 4: Comparison between patients with early surgical intervention after 1 CUS image and those who underwent intervention after 2 CUS images* Characteristic Early CSF Diversion p Value no. of patients GA in wks at birth 27.5 (3.1) 26.1 (2.6) 0.18 GA in wks at time of diversion 31.1 (3.3) 31.4 (3.2) 0.80 birth weight in g (469.0) (298.8) 0.11 initial hemorrhage category resolved 5 (14.3%) 0 (0%) 0.57 Grade I or II 3 (8.6%) 1 (10%) 1.00 Grade III or IV 27 (77.1%) 9 (90%) 0.66 ER initial 0.61 (0.11) 0.50 (0.13) <0.01 before CSF diversion 0.61 (0.11) 0.57 (0.11) 0.22 HC in cm initial 29.0 (3.0) 25.8 (4.0) <0.01 before CSF diversion 29.0 (3.0) 26.7 (1.8) no. of scans before CSF diversion 1 (0) 4.0 (2.4) <0.001 * Demographic and measured data for patients who received early surgical intervention, defined as CSF diversion after 1 CUS, compared to patients with later surgical intervention. Both HC and ER were significantly smaller in patients who underwent delayed CSF diversion (p < for both measures). Although initial ER measurements differed significantly between the 2 groups, the ER on the last scan before diversion did not differ significantly between the early diversion and delayed surgery groups. The HC measurements remained significantly different prior to diversion, regardless of whether patients underwent diversion early or late (p = 0.034). Unless otherwise indicated, the numbers in parentheses represent the SD. Significant differences (p < 0.05) are in boldface. At least 2 CUSs were done before VAD placement. Late VPS or VAD at a later time. Future work on identifying baseline characteristics of patients with IVH who develop progressive hydrocephalus would allow this subgroup to be identified and treated earlier. Weaknesses of This Study and Future Directions A weakness of our study is that other clinical indicators, such as fontanelle tension or apneic/bradycardic episodes, were not evaluated. Neurosurgeons do take these into account when determining the need for CSF diversion in infants, although these episodes are not always present, even with severe hydrocephalus. Although fontanelle tension has been shown to have good interrater reliability, there is no common method of measuring this tension quantitatively. 8,9 Correlation of our findings to measured fontanelle tension or actual ICP measurement would help determine whether ER or HC relates most closely to the elevated ICP. Patients who underwent late CSF diversion presented with significantly smaller ER and HC than those who underwent early CSF diversion. When these patients with socalled late CSF diversion were examined just prior to surgery, their ER, but not their HC, no longer differed from those in patients with so-called early CSF diversion. This suggests that clinicians may place more weight on ER than HC measurements when following patients over time. Alternatively, these patients hydrocephalus could have been slower progressing, and CSF diversion may have prevented them from developing HCs as large as the early CSF diversion group. It is important to note that an enlarging ER in the absence of increased HC or other signs of hydrocephalus could be due to parenchymal loss rather than hydrocephalus. This highlights the fact that a single clinical measurement should not be used in isolation to determine if patients require CSF diversion and that relying on ventricular size alone could lead to overtreatment. Additional work is needed to develop standardized clinical practices for CSF diversion in infants. Although our study did not show a correlation between HC measurements and ER, it is possible that our retrospective design was not optimally suited for this, because CUSs were performed at nonstandardized intervals. Prospective trials with clinical assessments of the anterior fontanelle timed closely with CUS studies could better determine if clinical assessments of the fontanelle can be sensitive enough to predict development of hydrocephalus. Additionally, emerging research has emphasized the potential for using MRI flow monitoring to predict relative responses to CSF diversion. 2 Continued investigation into these diagnostic assessments may lead to improved evaluation of IVH and allow for decreased incidence and morbidity of associated hydrocephalus. Conclusions Despite the realization that hydrocephalus leads to 188 J Neurosurg: Pediatrics / Volume 14 / August 2014
6 Head circumference and ultrasound findings poor clinical outcomes and impaired cognitive function, there is no standardized way to evaluate the efficacy of shunt placement by an institution. 3 Ultimately, the standardization of criteria for which patients undergo CSF diversion or other treatments for hydrocephalus, and the confirmation that these standards are efficacious, could lead to an efficient protocol for placing VPSs in neonates. Such improvements in treatment algorithms could reduce unnecessary testing and subjective test interpretations, and could potentially improve overall outcomes for infants with IVH. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Miller. Acquisition of data: Ingram, Huguenard. Analysis and interpretation of data: Miller, Ingram, Huguenard. Drafting the article: Ingram. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Miller. Statistical analysis: Ingram, Huguenard. Ad min i- strative/technical/material support: Chern. Study supervision: Miller, Chern. References 1. Aquilina K: Intraventricular haemorrhage in the newborn. Adv Clin Neurosci Rehabil 11:22 24, Bradley WG Jr, Whittemore AR, Kortman KE, Watanabe AS, Homyak M, Teresi LM, et al: Marked cerebrospinal fluid void: indicator of successful shunt in patients with suspected normal-pressure hydrocephalus. Radiology 178: , Brouwer A, Groenendaal F, van Haastert IL, Rademaker K, Hanlo P, de Vries L: Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for post-hemorrhagic ventricular dilatation. J Pediatr 152: , Brouwer M: Treatment and Outcome of Neonatal Haemorrhagic Brain Injury [dissertation]. Utrecht, The Netherlands: Utrecht University, de Vries LS, Liem KD, van Dijk K, Smit BJ, Sie L, Rademaker KJ, et al: Early versus late treatment of posthaemorrhagic ventricular dilatation: results of a retrospective study from five neonatal intensive care units in The Netherlands. Acta Paediatr 91: , Dykes FD, Dunbar B, Lazarra A, Ahmann PA: Posthemorrhagic hydrocephalus in high-risk preterm infants: natural history, management, and long-term outcome. J Pediatr 114: , Evans WA Jr: An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neurol Psychiatry 47: , Gross SJ, Oehler JM, Eckerman CO: Head growth and developmental outcome in very low-birth-weight infants. Pediatrics 71:70 75, Kaiser AM, Whitelaw AG: Intracranial pressure estimation by palpation of the anterior fontanelle. Arch Dis Child 62: , Kulkarni AV, Drake JM, Armstrong DC, Dirks PB: Measurement of ventricular size: reliability of the frontal and occipital horn ratio compared to subjective assessment. Pediatr Neurosurg 31:65 70, Müller WD, Urlesberger B: Correlation of ventricular size and head circumference after severe intra-periventricular haemorrhage in preterm infants. Childs Nerv Syst 8:33 35, Papile LA, Burstein J, Burstein R, Koffler H: Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 92: , Riva-Cambrin J, Shannon CN, Holubkov R, Whitehead WE, Kulkarni AV, Drake J, et al: Center effect and other factors influencing temporization and shunting of cerebrospinal fluid in preterm infants with intraventricular hemorrhage. Clinical article. J Neurosurg Pediatr 9: , Stonestreet B: Intraventricular hemorrhage in premature infants. Cerebrospinal Fluid Res 6:S3, Taylor GA, Madsen JR: Neonatal hydrocephalus: hemodynamic response to fontanelle compression correlation with intracranial pressure and need for shunt placement. Radiology 201: , Volpe JJ: Brain injury in the premature infant. Neuropathology, clinical aspects, pathogenesis, and prevention. Clin Perinatol 24: , Volpe JJ: Neurology of the Newborn, ed 5. Philadelphia: Saunders/Elsevier, Wellons JC III, Holubkov R, Browd SR, Riva-Cambrin J, Whitehead W, Kestle J, et al: The assessment of bulging fontanel and splitting of sutures in premature infants: an interrater reliability study by the Hydrocephalus Clinical Research Network. Clinical article. J Neurosurg Pediatr 11:12 14, 2013 Manuscript submitted November 26, Accepted May 8, Please include this information when citing this paper: published online June 20, 2014; DOI: / PEDS Address correspondence to: Brandon A. Miller, M.D., Ph.D., Department of Neurosurgery, Emory University, 1365 Clifton Rd. NE, Bldg. B, Ste. 2200, Atlanta, GA brandon.miller@ emory.edu. J Neurosurg: Pediatrics / Volume 14 / August
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