Retinal Findings in Young Children with Increased Intracranial Pressure from Nontraumatic Causes Angell Shi, BS,A Abhaya Kulkarni, MD, FRCSC,B Kenneth W

Retinal Findings in Young Children With Increased Intracranial Pressure From Nontraumatic Causes Angell Shi, BS,a Abhaya Kulkarni, MD, FRCSC,b Kenneth W. Feldman, MD,c Avery Weiss, MD,d Emily A. McCourt, MD,e Susan Schloff, MD,f,g Michael Partington, MD,h Brian Forbes, MD, PhD,i Brooke E. Geddie, DO,j Karin Bierbrauer, MD,k Paul H. Phillips, MD,l,m David L. Rogers, MD,n Waleed Abed Alnabi, MD,o,p Gil Binenbaum, MD, MSCE,i Alex V. Levin, MD, MHSca,o

OBJECTIVES: Increased intracranial pressure (ICP) has been suggested in legal settings as an abstract alternative cause of retinal hemorrhages (RHs) in young children who may have sustained abusive head trauma. We assessed the prevalence and characteristics of RHs in children with increased ICP. METHODS: We conducted a prospective, multicenter study of children ,4 years old with newly diagnosed increased ICP as determined by using direct measurement and/or clinical criteria. Infants who were premature, neonates, and suspected survivors of abusive head trauma were excluded on the basis of nonocular findings. Fundus examinations were performed; extent, number, and type of RH in each of 4 distinct retinal zones were recorded. RESULTS: Fifty-six children (27 boys) were studied (mean age 15.4 months; range 1–43 months). All of the children had elevated ICP that required intervention. One child had papilledema. No child (0%; 95% confidence interval: 0%–6.4%) or eye (0%; 95% confidence interval: 0%–3.3%) was found to have an RH. Causes of increased ICP included hydrocephalus, intraventricular hemorrhage, congenital malformations, malfunctioning shunts, and the presence of intracranial space-occupying lesions. CONCLUSIONS: Although acute increased ICP can present in children with a pattern of peripapillary superficial RHs in the presence of papilledema, our study supports the conclusion that RHs rarely occur in the absence of optic disc swelling and do not present beyond the peripapillary area in the entities we have studied.

aSidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, Pennsylvania; bDivision of WHAT’S KNOWN ON THIS SUBJECT: Although the Neurosurgery, The Hospital for Sick Children, Toronto, Ontario, Canada; Departments of cPediatrics and literature suggests that retinal hemorrhages (RHs) dOphthalmology, Seattle Children’s Hospital and School of Medicine, University of Washington, Seattle, beyond the peripapillary region are rare in children e Washington; Department of Ophthalmology, Children’s Hospital Colorado and School of Medicine, University of with increased intracranial pressure, the formation of Colorado, Aurora, Colorado; fAssociated Eye Care, St Paul, Minnesota; gDepartment of Ophthalmology and Visual Neurosciences, Children’s Minnesota St Paul Hospital, St Paul, Minnesota; hDepartment of Neurosurgery, Gillette widespread RHs in such children is often contested in Children’s Specialty Healthcare, St Paul, Minnesota; iDivision of Ophthalmology, Children’s Hospital of Philadelphia, legal proceedings regarding alleged abusive head Philadelphia, Pennsylvania; jDivision of Pediatric Ophthalmology, Helen DeVos Children’s Hospital, Grand Rapids, trauma. Michigan; kDivision of Pediatric Neurosurgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; lHarvey and Bernice Jones Eye Institute, University of Arkansas for Medical Sciences, Little Rock, Arkansas; WHAT THIS STUDY ADDS: Increased intracranial mDepartment of Ophthalmology, Arkansas Children’s Hospital, Little Rock, Arkansas; nDepartment of pressure due to the entities we studied is an unlikely o Ophthalmology, Nationwide Children’s Hospital, Columbus, Ohio; Department of Pediatric Ophthalmology and isolated cause of RHs beyond the peripapillary and Ocular Genetics, Wills Eye Hospital, Philadelphia, Pennsylvania; and pMédecins Sans Frontieres, Amman, Jordan prepapillary hemorrhages sometimes seen with Drs Feldman, Weiss, McCourt, Schloff, Partington, Binenbaum, Forbes, Geddie, Bierbrauer, Phillips, papilledema. and Rogers collected data and reviewed and revised the manuscript; Dr Abed Alnabi analyzed the data and reviewed and revised the manuscript; Ms Shi drafted the initial manuscript, analyzed the To cite: Shi A, Kulkarni A, Feldman KW, et al. Retinal data, and reviewed and revised the manuscript; Dr Kulkarni contributed to the design of the study, Findings in Young Children With Increased Intracranial collected data, and reviewed and revised the manuscript; Dr Levin conceptualized and (Continued) Pressure From Nontraumatic Causes. Pediatrics. 2019; 143(2):e20181182

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 143, number 2, February 2019:e20181182 ARTICLE A limited body of current published TABLE 1 Patient Recruitment measurements of ICP. Children who literature indicates that increased Site No. were included on the basis of clinical intracranial pressure (ICP) does not Children criteria exhibited (1) an egress of cause retinal hemorrhages (RHs) in Enrolled cerebrospinal fluid (CSF) under children except for the peripapillary Seattle Children’s Hospital 16 pressure during a surgical and prepapillary hemorrhages Children’s Hospital Colorado 8 intervention and/or brain imaging associated with papilledema.1,2 The Hospital for Sick Children 7 that revealed a space-occupying Gillette Children’s Specialty 6 Despite this evidence, increased ICP Healthcare lesion (or multiple lesions), cerebral continues to be implicated in legal Children’s Hospital of Philadelphia 5 edema, and/or hydrocephalus and (2) settings as an alternative cause of Cincinnati Children’s Hospital 4 $1 symptoms or signs indicative of RHs by the defense when young Medical Center elevated ICP, including headache, ’ children are thought to have been Helen DeVos Childrens Hospital 4 vomiting, cranial nerve VI palsy, Arkansas Children’s Hospital 3 survivors of abusive head trauma Nationwide Children’s Hospital 3 lethargy and/or drowsiness, (AHT).2 Attorneys often extrapolate conjugate downward deviation from older studies with adult subjects (“sunsetting”) of the eyes, tense 3,4 were identified by an on-site to support this claim, misuse fontanelle or splayed sutures, investigator or contact person in the studies to suggest that increased ICP clinical indicators of a failed neurosurgical service, general can frequently cause widespread RHs ventricular shunt, and characteristic 2,5–7 pediatric service, or PICU within in children, or cite what they neuroimaging and/or optic disc 24 hours of admission. Given that believe to be an inadequate body of swelling. When possible, ICP was families were to be approached so literature to the contrary in children. also measured by using CSF shunt early in their hospital stay and at Because accurate diagnoses are of manometry or an intraventricular a time when they may have been in critical importance in evaluations of monitor. A direct ICP measurement crisis because of the acutely elevated child abuse, a broad evidence base is of $25 cm H O was used as a ICP in their children, possible 2 essential for clinicians to quantitative criterion for inclusion. impending surgery, and/or a new appropriately interpret potential This level was chosen on the basis of diagnosis, the primary inpatient findings of RH in cases of increased clinical expertise because there was attending physician was responsible ICP. Increasing the evidence base is no definitively established threshold for clearing the patients to have their essential for both the bedside and the for abnormally high ICP in infants families be approached for courtroom. Our purpose in this study and toddlers at the onset of the participation in the study. Therefore, was to assess the prevalence and study. Infants ,1 year of age who an eligible patient was only excluded characteristics of RHs associated with were born before 36 weeks’ gestation, when the attending physician felt that increased ICP in children through neonates ,4 weeks postpartum, the family was not emotionally in a prospective investigation of the and children who were diagnosed a position to offer adequate consent. ocular findings in a sample of by a multidisciplinary team as being Some patients may have been missed children with acute increased ICP survivors of AHT independent of because of a failure to identify from causes other than child abuse. the eye findings were excluded. potentially eligible patients or unavailability of study staff to obtain Child age and sex, medical history, METHODS consent or conduct an ophthalmic ophthalmologic examination findings, We conducted a prospective, examination during the designated brain imaging findings, ICP fi multicenter study of fundus critical periods de ned in the study. measurements, and the duration of examinations in children ,4 years of Data were not collected on unenrolled elevation for increased ICP (if age with increased ICP from March patients. Given the study structure, available) were collected from the 2008 to February 2017. The study we believe it unlikely that the study medical record, deidentified, and sent was approved by the Wills Eye sample was biased but rather that it to the data collection center by using Hospital Institutional Review Board represented a random sampling of fax or e-mail. Consent was not (the data collection center) and by the eligible patients who were able to be required for the eye examination institutional review boards of each of enrolled. Consent for the release of because it was believed at the fi the 9 participating sites (Table 1). deidenti ed data was obtained for all participating sites to be routine care Because sites were accepted for enrolled children; no child was for children with increased ICP. participation on a rolling basis, the excluded because consent was Informed consent was obtained from length of recruitment at each site denied. at least 1 parent or guardian for all varied. Inclusion required that Increased ICP was determined by enrolled children who met the study eligible patients with increased ICP using clinical criteria and/or direct criteria to allow for the disclosure of

Downloaded from www.aappublications.org/news by guest on September 27, 2021 2 SHI et al the deidentified data from their TABLE 2 Subject Demographics of 56 Children for RHs. In the 2 children with ophthalmic and neurosurgical care With Raised ICP hypertension, no signs of providers to the data collection site. No. hypertensive retinopathy (vascular The consent discussion included the Children changes or exudates) were noted on disclosure of the possibility of an Age, moa examination. Hypertension has not investigation for AHT should retinal 1–515been reported as a cause of isolated examination reveal findings that 6–11 12 RHs in young children. No child had 12–23 13 might be concerning for possible a confounding condition, such as 24–35 10 child abuse. 36–43 6 hyponatremia, hypernatremia, or Sex coagulopathy. All 56 children met the Ophthalmologists at each site Male 27 clinical criteria for increased ICP performed retinal examinations by Female 29 defined above and were therefore using indirect ophthalmoscopy a The mean age for all children was 15.4 months. eligible for inclusion in the study on through pathologically or the basis of clinical criteria alone. pharmacologically dilated pupils on summarized in Table 3. Three Reliable, direct ICP measurements each child. When the pupils were not children had concurrent conditions, ranging from 25 to 50 cm H O were pathologically dilated, the decision to 2 including hypertension (2 children) also obtained in 7 children, who had use mydriatic eye drops (1 drop each and coronavirus upper-respiratory a mean ICP reading of 28.9 cm H O of cyclopentolate or tropicamide 1% 2 infection (1 child), which were not and therefore met quantitative and phenylephrine 2.5%) with or considered to be potential risk factors criteria for inclusion in addition to without proparacaine 0.5% was clinical criteria. Twelve children had based on the medical team’s unreliable ICP measurements that assessment of each child’s clinical TABLE 3 Clinical Findings of Increased ICP were made only after a neurosurgical state. If dilation was felt to be Among 56 Children With Raised ICP release of CSF had already occurred, contraindicated, an attempt was No. resulting in values that were assumed made to examine the retina without Children to be falsely reduced by an dilation. Children for whom the Direct measurement of ICP 19 indeterminable amount because of retinal view was inadequate were CSF shunt manometry 9 the preceding release of CSF. excluded from the study. The extent, Intraventricular monitor 9 Measurements were obtained by number, and type of RH in 4 distinct Method unknown 1 Clinical criteria 53 using CSF shunt manometry in 9 zones of the retina (A, peripapillary; Vomiting 27 children and intraventricular ICP B, posterior pole excluding the Lethargy and/or drowsiness 19 monitors (including external peripapillary zone; C, peripheral Tense fontanelle or splayed 18 ventricular drainage devices) in 9 retina posterior to a circle through sutures children. The method of ICP the vortex veins; and D, peripheral Headache 9 Sunsetting of eyes 9 measurement was not recorded retina anterior to the vortex veins and Papilledema 9 for 1 child. No child had an extending to the ora serrata) were Cranial nerve VI palsy 1 intraparenchymal or subarachnoid assessed by using a previously tested Other clinical signs of increased ICP a bolt. The estimated duration of ICP description system.8 CSF egress 8 Increased head circumference 8a elevation in most children was on the Standard descriptive statistics were Irritability and/or fussing 5 scale of weeks (with a range from a calculated. The primary outcome was Paresthesias and/or weakness of 4 ,12 hours to 6–8 months in 1 the prevalence of RHs, which was the extremities Decreased oral intake 3 patient), but all children, including calculated as the proportion of Decreased gross motor skills 1 those with chronic or intermittently children and proportion of eyes with Progressive loss of balance 1 elevated ICP, had acutely elevated ICP RHs among all examined children. Head tilt 1 at the time of their admission that The Wilson9 method was used to Gaze abnormalities 1 required intervention. calculate the 95% confidence Seizures 1 Estimated length of time ICP elevated intervals (CIs) for the prevalence Hours 4 The etiologies of elevated ICP are of RHs. Days 17 summarized in Table 4. We had no Weeks 27 children who presented with Uncertain 8 increased ICP caused by trauma. RESULTS Patients may have qualified for a diagnosis of increased Imaging findings revealed Fifty-six children were enrolled ICP on the basis of both clinical criteria and/or direct hydrocephalus or ventriculomegaly in measurement. (Table 2). Their clinical and ICP a In 3 patients, the specified clinical sign was noted to be 45 children and the presence of measurement findings are the only indicator of increased ICP. a mass, tumor, or cyst in 18 children.

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 143, number 2, February 2019 3 TABLE 4 Causes of Increased ICP retina, involving any geographic area Cause No. from the peripapillary region to the Children ora serrata. In most patients, RHs are Brain tumor 15 too numerous to count and Primary hydrocephalusa 15 widespread in distribution.10,13 Shunt obstruction 12 Increased ICP is a theory frequently Secondary hydrocephalus 16 proffered in legal settings as an Arteriovenous malformationb 2 Chiari malformation 3 alternative cause of severe RHs, Craniosynostosis 3 usually in suspected cases of AHT. Dandy-Walker malformation (Joubert syndrome) 1 However, to our knowledge, no study Intraventricular cyst 1 in children has demonstrated that b Intraventricular hemorrhage 2 elevated ICP causes RHs beyond Previous meningococcal disease and/or encephalitisa 2 Subdural hygroma 1 those associated with papilledema in Cerebral edema (birth anoxia with previous subdural and subarachnoid hemorrhage) 1 the prepapillary or peripapillary 1,2 a One child had both bacterial meningitis and hydrocephalus. distribution, except for situations in b One child had intraventricular hemorrhage from an arteriovenous malformation. which hyperacute rises in ICP occur, such as fatal head crushing,14–16 fatal motor vehicle crashes,17–19 ruptured 6,7,20 21 Intraventricular hemorrhage was although there were no RHs in zones aneurysms, or a fall of 11 m. seen in 2 children. In 13 children, $1 A, B, or C, which comprise the Although medical conditions such as congenital malformation (type 1 majority of the retina. Additionally, leukemia, coagulopathy, or sepsis may 22 Chiari malformation, schizencephaly, for 2 children, details of the also produce RHs, they are typically encephalocele, cerebellar hypoplasia, examination (ie, the quality of retinal less severe. All of these conditions are hydranencephaly, Dandy-Walker view) were not provided, although readily obvious on the basis of variant, syrinx, syringomyelia, and there were no RHs noted in the history, basic laboratory testing, or 10 myelomeningocele) were seen. When assessment of any of the 4 zones. neuroradiology. As such, these appropriate, distinctions were made Successful pharmacologic dilation of recognizable entities cause little if any between imaging findings and both eyes was achieved in all but 2 confusion regarding a diagnosis etiologies of elevated ICP; the children, 1 of whom was dilated in of AHT. fl etiologies noted in Table 4 re ect the the left eye only but received a None of our subjects had RHs. A view cause of elevated ICP at the time of bilateral fundus examination. In the of the entire retina was obtained in ’ the child s presentation. For example, other child, a good view of the 91% of children. A full view of the far 2 children presented with posterior pole in both eyes was retinal periphery (zone D) could not hydrocephalus due to shunt obtained without dilation. Although 9 be obtained in 5 children. We believe obstruction; these shunts had been children were noted to have it is unlikely that RHs would be placed previously for hydrocephalus papilledema (a clinical sign of present in this most anterior zone yet that was caused by an intracranial increased ICP) by a nonophthalmologist, absent in the other 3 zones that cyst. In these patients, the elevation results from an evaluation comprise the majority of the retina, in ICP was attributed to the shunt conducted by an ophthalmologist especially because RHs from obstruction rather than the cysts, revealed optic disc swelling in increased ICP are typically found on although the latter were still noted on 1childwhoalsodidnothaveany or around the optic nerve in imaging. RH. association with optic disc swelling. No child was found to have RHs in Our findings are consistent with those DISCUSSION any zone of the retina. The prevalence previously reported. In a study of 17 was 0% in any child (95% CI: RHs in young children are infants with increased ICP due to 0%–6.4%) and 0% in any eye (95% a significant and well-established obstructive hydrocephalus, cerebral CI: 0%–3.3%). In 51 of 56 children, indicator of potential AHT, resulting edema, spontaneous intracranial there was documentation of an from repeated acceleration and hemorrhage, or extraaxial effusion, adequate assessment of all 4 retinal deceleration with or without blunt the authors concluded that increased zones, including the posterior pole head impact (also referred to as ICP without intracranial hemorrhage (zones A and B) and peripheral retina “shaken baby syndrome”).10 RHs are did not appear to cause severe RHs.23 (zones C and D). In 5 children, the present in ∼85% of survivors,11 In survivors of AHT, there was no assessment of zone D (the outermost frequently bilateral,11,12 and most correlation between increased ICP peripheral retina) was suboptimal, often located in multiple layers of the and RHs.11 Of children with a shunt

Downloaded from www.aappublications.org/news by guest on September 27, 2021 4 SHI et al malfunction and a corresponding children with AHT and increased ICP nerve sheath hemorrhages can occur increased ICP, ∼14% demonstrate (14 of 14) and 4 of 7 children with after acute increases in ICP,3,4,27 these papilledema, but RHs have not been AHT without increased ICP had RH findings are not always generalizable noted.24,25 Although the findings in (total 86%; 18 of 21 children). This to children.2,28 Anatomic and older literature may suggest an compares with the children with physiologic differences between the association of RHs with conditions unintentional traumatic brain injuries eyes of adults and children, that cause increased ICP,26 many of (TBIs); 18% of children (6 of 34) with particularly in the retinal vasculature these studies were conducted at increased ICP and 4% of children (1 of and the strength of vitreoretinal a time before AHT was recognized as 23) without increased ICP had RH attachments, must be considered a possible etiology. (total 12%; 7 of 57 children). along with differences in the etiology Insufficient data are given regarding and nature of the raised ICP. The Recent publications have clearly the number or pattern of RHs in the authors of 1 study of increased ICP demonstrated the pattern of RHs seen children who were not abused, thus found postmortem optic nerve sheath with isolated increased ICP, including limiting interpretation of their results. hemorrhages in 87% of eyes (40 of idiopathic intracranial hypertension. Because the types and severities of 46) and intraocular hemorrhages in Binenbaum et al1 found a small trauma and the underlying diseases 37% of eyes (17 of 46). They percentage (16%) of RHs among 100 were not specified for the children concluded that these hemorrhages children with nontraumatic elevated with unintentional trauma and the were the result of ruptured intradural ICP but only in the presence of optic children with nontraumatic and bridging vessels and obstructions disc swelling; all of these were encephalopathy and RHs, respectively, of the central retinal vein and splinter and/or superficial it cannot be determined if their retinochoroidal anastomoses.3 Patient intraretinal peripapillary underlying illnesses and injuries, such ages were not specified, but the hemorrhages and were limited to the as motor vehicle crashes17 or article comes from an institution in area on or around the optic disc. leukemia, could be expected to cause which only adults are treated. In Differences in subject age and cause RHs. The authors found no significant addition, all of the systemic diagnoses of increased ICP between Binenbaum association between ICP (as involved significant cerebral et al’s1 study and ours may explain determined by using direct compression (severe cerebral trauma, why we found only 1 case of measurement only) and either the spontaneous intracerebral papilledema and no papilledema- prevalence or number of RHs. hemorrhage, ruptured berry related RHs in our subjects. For Although they did find a statistically aneurysm, and internal carotid example, the most frequent cause of significant association between raised occlusion resulting in cerebral increased ICP in their study was ICP (as determined by using direct swelling without hemorrhage). These idiopathic intracranial hypertension measurement or clinical and/or diagnoses are far more common in (70% of patients), whereas we had no radiologic signs) and RHs, the authors adults and were not seen in any of patients with this etiology in our note that they cannot establish our patients. In another study, study. The prevalence of RHs and causation. In addition, this association subhyaloid hemorrhages after papilledema also appears to be higher was based on an analysis of patients in subarachnoid, subdural, and in older children with fused cranial which researchers did not distinguish extradural hemorrhages were seen in sutures; the age range of children in between children with inflicted TBIs 5 of 6 adults with repeated episodes our study was 1 to 43 months (mean (n = 14), unintentional TBIs (n = 34), of sudden increases in ICP4, which are 15.4 months) compared with 3 to and nontraumatic encephalopathy circumstances that rarely if ever 17 years (mean 12 years) in the (n = 15). Because increased ICP is occur in children without previous study. frequently seen in inflicted TBI, the a corresponding history. Minns et al5 found RHs in 38% of mixing of these samples will skew the children (24 of 63) with raised ICP analysis. The largest number of RHs Those who have claimed that more (as determined by using direct was found in patients with inflicted widespread hemorrhages can occur measurement, radiologic signs, or TBIs; the authors concluded that the because of raised ICP base their clinical signs) from a variety of RHs in these patients “occurred at the hypotheses on a presumed causes. In children with nontraumatic time of the traumatic acceleration/ obstruction of venous outflow in the encephalopathy and raised ICP, the deceleration injury” and were unlikely central retinal vein and a resulting incidence of RHs was 27% (4 of 15 to have been exacerbated by increase in central venous pressure. children); all subjects with RHs increased ICP. Central retinal vein occlusion lacked specific ICP measurements (4 presents with a distinct pattern of of 9 children) and specifications of Although studies in adults have retinal bleeding along with dilated the cause of their encephalopathy. All suggested that intraocular and optic and tortuous retinal veins.29 In

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 143, number 2, February 2019 5 a study of 17 children with a hyperacute ICP rise. In all others, children with isolated increased ICP nontraumatic increased ICP, there estimates ranged from hours to should be studied. If increased ICP is were no patients with retinal venous months. In children whose ICP had indeed able to cause RHs beyond the dilation.23 The anatomy of retinal been elevated for weeks or months, peripapillary area, then it should be vasculature should prevent the hyperacute increases could have able to do so regardless of etiology. formation of RHs in that there are perhaps occurred transiently, collateral pathways for venous producing RHs that resolved before CONCLUSIONS drainage through the vortex veins and their admission and study enrollment. retinochoroidal anastomoses.2,3 However, preretinal and subretinal In our study of 56 children with Additionally, RHs are not seen in hemorrhages often take several increased ICP due to primary and many other conditions that cause weeks to resolve, and if these types of secondary hydrocephalus, shunt increases in central venous pressure, hemorrhage had indeed occurred, obstruction, brain tumors, and such as severe cough, vomiting, they likely would have been seen on cerebral edema, we found no cases of seizures, or cardiopulmonary examination. In addition, all of our increased ICP causing RH regardless resuscitation with chest subjects had ICPs elevated enough to of the etiology of increased ICP, age of compressions.2,30–33 require admission and/or surgical the child, or duration of ICP elevation intervention at the time of their eye and despite a clinical severity of Our study had certain limitations. examinations. The absence of increased ICP in all children that Enrollment over the 9-year study papilledema in almost all of our warranted intervention. Although period was limited because of subjects can also be used to argue acute increased ICP can present a failure to identify potentially that their increased-ICP onsets of in children with a pattern of eligible patients, determinations by 34,35 peripapillary superficial RH in the concern were acute. Increased 1 the primary attending team that ICP was diagnosed clinically in presence of papilledema, with our families were not appropriate to be all subjects, although a minority results, we provide clear evidence to approached for consent during the of our subjects had direct ICP support the conclusion that RHs ’ acute phases of their children s care, measurements, and of these, many rarely occur in the absence of optic and a lack of on-site investigator were felt to be unreliable. Obtaining disc swelling and do not present availability either for recruitment accurate ICP measurements was not beyond the peripapillary area in the from the neurosurgical service always possible given the necessity of entities we have studied. and/or PICU or regarding ability CSF drainage in many patients with to perform ophthalmologic acutely elevated ICP, particularly ACKNOWLEDGMENT examinations before patient because higher ICP values induce We thank Gui-Shuang Ying for his discharge, resulting in a small sample substantial artifactual reductions in size. We believe the children included assistance in the statistical analysis of measured ICP at both rapid and the data. in this study are unlikely to represent reduced rates of drainage.36 a biased selection given the random Intraoperative confirmation of nature of these exclusions. We also increased ICP was often made ABBREVIATIONS did not have any patients present visually by the investigator rather with hyperacute sudden elevations in than by using objective measurement. AHT: abusive head trauma ICP. Although an approximate CI: confidence interval duration of increased ICP was We did not include children with AHT CSF: cerebrospinal fluid obtained for most children, the length who had increased ICP to avoid ICP: intracranial pressure of time was unknown in 8 children; confounding etiologies of RH. To RH: retinal hemorrhage however, they had mechanisms that evaluate the potential of increased TBI: traumatic brain injury would not be expected to result in ICP as a cause of RH, a population of

designed the study, coordinated and supervised data collection and analysis, drafted the initial manuscript, and reviewed and revised the manuscript; and all authors approved the ﬁnal manuscript as submitted and agree to be accountable for all aspects of the work. DOI: https://doi.org/10.1542/peds.2018-1182 Accepted for publication Nov 14, 2018 Address correspondence to Alex V. Levin, MD, MHSc, Pediatric Ophthalmology and Ocular Genetics, Wills Eye Hospital, 840 Walnut St, Suite 1210, Philadelphia, PA 19107. E-mail: [email protected]

Downloaded from www.aappublications.org/news by guest on September 27, 2021 6 SHI et al PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2019 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no ﬁnancial relationships relevant to this article to disclose. FUNDING: Funded in part by the Foerderer Fund (Dr Levin), the Robison D. Harley, MD, Endowed Chair in Pediatric Ophthalmology and Ocular Genetics (Dr Levin), and the National Eye Institute (grant K12 EY-015398; Dr Binenbaum). Funded by the National Institutes of Health (NIH). POTENTIAL CONFLICT OF INTEREST: Drs Levin and Feldman have provided paid expert testimony in child abuse cases; the other authors have indicated they have no potential conﬂicts of interest to disclose.

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Downloaded from www.aappublications.org/news by guest on September 27, 2021 8 SHI et al Retinal Findings in Young Children With Increased Intracranial Pressure From Nontraumatic Causes Angell Shi, Abhaya Kulkarni, Kenneth W. Feldman, Avery Weiss, Emily A. McCourt, Susan Schloff, Michael Partington, Brian Forbes, Brooke E. Geddie, Karin Bierbrauer, Paul H. Phillips, David L. Rogers, Waleed Abed Alnabi, Gil Binenbaum and Alex V. Levin Pediatrics originally published online January 10, 2019;

Updated Information & including high resolution figures, can be found at: Services http://pediatrics.aappublications.org/content/early/2019/01/08/peds.2 018-1182 References This article cites 35 articles, 10 of which you can access for free at: http://pediatrics.aappublications.org/content/early/2019/01/08/peds.2 018-1182#BIBL Subspecialty Collections This article, along with others on similar topics, appears in the following collection(s): Neurology http://www.aappublications.org/cgi/collection/neurology_sub Neurological Surgery http://www.aappublications.org/cgi/collection/neurological_surgery_ sub Ophthalmology http://www.aappublications.org/cgi/collection/ophthalmology_sub Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.aappublications.org/site/misc/Permissions.xhtml Reprints Information about ordering reprints can be found online: http://www.aappublications.org/site/misc/reprints.xhtml

Downloaded from www.aappublications.org/news by guest on September 27, 2021 Retinal Findings in Young Children With Increased Intracranial Pressure From Nontraumatic Causes Angell Shi, Abhaya Kulkarni, Kenneth W. Feldman, Avery Weiss, Emily A. McCourt, Susan Schloff, Michael Partington, Brian Forbes, Brooke E. Geddie, Karin Bierbrauer, Paul H. Phillips, David L. Rogers, Waleed Abed Alnabi, Gil Binenbaum and Alex V. Levin Pediatrics originally published online January 10, 2019;

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/early/2019/01/08/peds.2018-1182

Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. Pediatrics is owned, published, and trademarked by the American Academy of Pediatrics, 345 Park Avenue, Itasca, Illinois, 60143. Copyright © 2019 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.

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