J Neurosurg Pediatrics 14:184–189, 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 Department of Neurosurgery, Emory University; and 2Pediatric Neurosurgery Associates at Children’s Healthcare of Atlanta, Georgia

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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. (http://thejns.org/doi/abs/10.3171/2014.5.PEDS13602)

Key Words      •      intraventricular hemorrhage      •      hydrocephalus      • cranial ultrasound      •      head circumference      •      prematurity

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ntraventricular 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.

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< 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 J Neurosurg: Pediatrics / Volume 14 / August 2014

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. Patient Selection

Methods

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 mea­surements, and radiographic findings are shown in Ta­ble 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 = 0.029 and 0.041, respectively).

Correlation Between ER and HC

We used a correlation analysis to determine if HC 185

M. C. E. Ingram et al. TABLE 1: Comparison between demographic data in patients receiving CSF diversion and those who underwent no surgical diversion* Surgical CSF Diversion Quality on Presentation

No

Yes

p Value†

no. of patients GA in wks at birth birth weight in g GA in wks at initial assessment hemorrhage category  resolved   mild-moderate (Grade I or II)   severe (Grade III or IV) initial ER  overall   resolved hemorrhage   mild-moderate hemorrhage   severe hemorrhage initial HC in cm  overall   resolved hemorrhage   mild-moderate hemorrhage   severe hemorrhage

99 27.4 (4.5) 1153.9 (784.3) 32.15 (24.5)

45 27.2 (3.0) 1058.2 (446.8) 29.51 (4.4)

0.79 0.45 0.48

6 (6.1%) 54 (54.5%) 39 (39.4%)

5 (11.1%) 4 (8.9%) 36 (80.0%)

0.32

Poor correlation between head circumference and cranial ultrasound findings in premature infants with intraventricular hemorrhage.

Intraventricular hemorrhage (IVH) is the most common cause of hydrocephalus in the pediatric population and is particularly common in preterm infants...
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