CLINICAL REPORT Guidance for the Clinician in Rendering Pediatric Care

Routine Neuroimaging of the Preterm Brain Ivan L. Hand, MD, FAAP,a Renée A. Shellhaas, MD, MS, FAAP,b Sarah S. Milla, MD, FAAP,c COMMITTEE ON FETUS AND NEWBORN, SECTION ON NEUROLOGY, SECTION ON RADIOLOGY

Neuroimaging of the preterm infant is a common assessment performed in abstract the NICU. Timely and focused studies can be used for diagnostic, therapeutic, and prognostic information. However, significant variability exists among a neonatal units as to which modalities are used and when imaging studies are Department of Pediatrics, New York City Health 1 Hospitals/Kings County, State University of New York Downstate Medical Center, obtained. Appropriate timing and selection of neuroimaging studies can help Brooklyn, New York; bPediatric Neurology Division, Department of identify neonates with brain injury who may require therapeutic intervention Pediatrics, Michigan Medicine, University of Michigan, Ann Arbor, Michigan; and cDepartments of Radiology and Pediatrics, Emory or who may be at risk for neurodevelopmental impairment. This clinical report University School of Medicine and Children’s Healthcare of Atlanta, reviews the different modalities of imaging broadly available to the clinician. Atlanta, Georgia

Evidence-based indications for each modality, optimal timing of examinations, Clinical reports from the American Academy of Pediatrics benefit from and prognostic value are discussed. expertise and resources of liaisons and internal (AAP) and external reviewers. However, clinical reports from the American Academy of Pediatrics may not reflect the views of the liaisons or the organizations or government agencies that they represent.

Drs Hand, Shellhaas, and Milla researched, conceived, designed, INTRODUCTION analyzed, and interpreted data for this clinical report and drafted and revised this clinical report; and all authors approved the final Central to the assessment of the preterm infant is identifying the presence manuscript as submitted. and extent of brain injury. Preterm infants are at significant risk of The guidance in this report does not indicate an exclusive course of intraventricular hemorrhage (IVH), periventricular leukomalacia (PVL), treatment or serve as a standard of medical care. Variations, taking into account individual circumstances, may be appropriate. posthemorrhagic ventricular dilatation, and other neurologic injuries that All clinical reports from the American Academy of Pediatrics may or may not have imaging corollaries. Through neuroimaging, the automatically expire 5 years after publication unless reaffirmed, neonatologist may initiate interventions and plan for supportive care and revised, or retired at or before that time. assess the risk of future neurologic impairment. This document is copyrighted and is property of the American 1 fi Academy of Pediatrics and its Board of Directors. All authors have filed In 1968, Abraham Towbin described the frequent nding of IVH at conflict of interest statements with the American Academy of necropsy in preterm infants, with abnormalities almost universally Pediatrics. Any conflicts have been resolved through a process ’ approved by the Board of Directors. The American Academy of present in those born at less than 28 weeks gestation. Not until 10 years Pediatrics has neither solicited nor accepted any commercial later did Papile at al2 describe the computerized tomography (CT) findings involvement in the development of the content of this publication. of 46 consecutive very low birth weight (VLBW) infants and demonstrate DOI: https://doi.org/10.1542/peds.2020-029082 a much higher incidence of IVH than was clinically suspected. That report Address correspondence to Ivan L. Hand, MD, FAAP. E-mail: ivan.hand@ described 4 separate grades of hemorrhage: “Grade I–subependymal nychhc.org hemorrhage, Grade II–intraventricular hemorrhage without ventricular – dilatation, Grade III intraventricular hemorrhage with ventricular To cite: Hand IL, Milla SS, AAP COMMITTEE ON FETUS AND dilatation, and Grade IV–intraventricular hemorrhage with parenchymal NEWBORN, SECTION ON NEUROLOGY, SECTION ON RADIOLOGY. hemorrhage.” Since the initial report, the Papile classification has been Routine Neuroimaging of the Preterm Brain. Pediatrics. modified to grade I, indicating minimal IVH; grade II, with IVH occupying 2020;146(5):e2020029082

Downloaded from www.aappublications.org/news by guest on October 2, 2021 PEDIATRICS Volume 146, number 5, November 2020:e2020029082 FROM THE AMERICAN ACADEMY OF PEDIATRICS 10% to 50% of the ventricular area; INITIAL SCREENING EXAMINATIONS IVH and, on the basis of current grade III, representing IVH with The VLBW (ie, birth weight ,1500 g) understanding, believed to be caused . 50% of ventricular area; and last, infant is at high risk for germinal by venous infarction. A PVHI is not, as parenchymal hemorrhage, most likely matrix and IVH as well as ischemic once believed, an extension of the IVH attributable to hemorrhagic venous fi into the parenchyma. 3 white matter injury as identi ed by infarction. cranial ultrasonography. Risk of Severity of IVH in the most immature fi severe IVH is inversely related to These ndings led to one of the infants is consistent with the 4 gestational age, with infants born at earliest outcomes studies, in which developmental changes of the less than 24 weeks’ gestation at authors described the association of subependymal germinal matrix as it highest risk.10 In 2017, the Vermont major developmental and decreases in size from 2.5 mm in the Oxford Network database neuromotor handicaps with the 24-week preterm infant to involution fi demonstrated an overall 24.6% ndings of more severe (grade III and at about 36 weeks’ gestational age.3 incidence of IVH and an 8.1% rate of IV) IVH on CT scan performed For these and other reasons affecting severe IVH, defined as grade III or IV between 3 and 10 days of age. On the vascular integrity, the more moderate basis of these and other studies, the among more than 50 000 VLBW 11 and late preterm infants (those born American Academy of Neurology infants. In a recently published between 32 and 36 6/7 weeks’ (AAN) released practice parameters survey of the California Perinatal gestation) are at less risk for in 2002 suggesting universal cranial Quality Care Collaborative, 63% of significant intracranial injury. In ultrasonographic screening for all infants born at 22 to 23 6/7 weeks’ a retrospective study of moderately infants born at less than 30 weeks’ gestation had IVH, with 36% 12 preterm infants born between 29 and gestation.5 The AAN also demonstrating severe IVH. This 33 weeks’ gestation, 60% of a cohort recommended that initial screening incidence decreased to 14% of infants of 7021 infants underwent cranial ultrasonography be performed at 7 to whose gestational age at birth was 30 imaging, and 15% of these 4184 14 days after birth and repeated at to 31 6/7 weeks having any IVH and infants had ultrasonographic near term corrected age. In 2001, the 1.4% having a severe grade. Less abnormalities.16 The rates of severe Canadian Pediatric Society severe grades of IVH (grades I and II) IVH and cystic PVL were 1.7% and recommended screening all infants may have less prognostic influence on 2.6%, respectively, in this born at less than 32 weeks’ gestation clinical outcomes. In a National population.15 The authors noted that at 2 weeks after birth, with a repeat Institute of Child Health and low Apgar scores, maternal risk screening 6 weeks after birth.6 Since Development study of 1472 infants factors, lack of antenatal steroids, and the publication of those guidelines, born at less than 27 weeks’ 13 vaginal delivery were associated with cranial ultrasonography capabilities gestational age, there was no ultrasonographic abnormalities, have evolved, and modern significant difference in including intracranial hemorrhage, ultrasonography technology, along neurodevelopmental outcomes at 18 PVL, and ventriculomegaly. The with the use of supplementary to 22 months of those infants with presence of risk factors such as acoustic windows, can now provide and without these low-grade abnormal neurologic examination, good structural imaging of the hemorrhages. intrauterine growth restriction, preterm infant brain.7 PVL is a disorder of the abnormal head circumference, low Imaging the entire brain was once periventricular cerebral white matter Apgar scores, and need for ventilation performed by using CT scanning. Use that may be cystic or diffuse in or surfactant increased the chance of of head CT has given way to improved nature. Most cystic PVL occurs in detecting an abnormality by fourfold cranial ultrasonography as well as infants born between 26 and 30 in a group of more mature preterm MRI, which yields better detail and weeks’ gestation, initially appearing infants born at 33 to 36 weeks’ avoids the use of ionizing radiation.8 as periventricular increased gestational age.17 In a similar study, However, routine use of MRI for echogenicity (eg, a blush or flare) infants born at .30 weeks’ gestation screening the preterm infant has been with cystic evolution over the course who were found to have significant identified as being of questionable of a few weeks. Periventricular ultrasonographic abnormalities value in the Choosing Wisely hemorrhagic infarcts (PVHIs) (ie, typically had clinically significant campaign of the American Academy formerly grade 4 IVH) occur mainly in events, such as placental abruption, of Pediatrics.9 The aim of this clinical infants born at ,26 weeks’ seizures, hypotension, and report is to provide guidance to gestation14 and occur infrequently in hydrocephalus, which warranted the clinicians for an evidence-based infants born beyond 30 weeks’ cranial ultrasonographic approach to neuroimaging for the gestation.15 A PVHI is a parenchymal investigations.18 Risk factors also play preterm infant. lesion usually associated with a large a role in the more immature preterm

Downloaded from www.aappublications.org/news by guest on October 2, 2021 2 FROM THE AMERICAN ACADEMY OF PEDIATRICS infants as well. In a study of 303 infant as increased echogenicity of a significantly higher primary infants born at ,30 weeks’ gestation, the periventricular white matter, outcome of late death or no asymptomatic infants required sometimes described as an echogenic neurodevelopmental impairment clinical intervention solely on the “blush” or “flare.” Because the than those who never had such basis of screening ultrasonography periventricular white matter may findings.28 Thus, even if the findings performed at 7 to 14 days.19 All normally have slight increased were transient, infants with cystic infants who required clinical echogenicity, the echogenic choroid PVL warrant close follow-up interventions had factors plexus can be used as an internal observation for neurodevelopmental precipitating an ultrasonographic comparison for increased impairment. Communication study, including anemia, metabolic echogenicity.25 Normal regarding neuroimaging results and acidosis, pulmonary hemorrhage, and periventricular white matter should follow-up plans are recommended hypotension. Similar results have be less echogenic than the choroid between inpatient and outpatient been reported for infants born at ,32 plexus. These areas of white matter providers. weeks’ gestation with risk factors for abnormality may become cystic on severe IVH including lack of antenatal ultrasonography within 2 to 5 weeks STANDARD CRANIAL ULTRASOUND steroids, outborn status, asphyxia, and/or lead to ventriculomegaly from IMAGING TECHNIQUE significant acidosis, and/or white matter volume loss, which can hypotension.10 Thus, the risk for be visible on repeat ultrasonography Cranial ultrasound imaging has severe IVH is associated with at term equivalent age (TEA). In light traditionally made use of the anterior gestational age #30 weeks’ gestation, of these findings, the Canadian fontanelle as an acoustic window and with the highest risk in infants born Pediatric Society recommended should be performed by an American at ,24 weeks’ gestation. Infants born screening at 6 weeks of age, whereas Registry for Diagnostic Medical at .30 weeks’ gestation have a low the AAN suggested a near term Sonography board-certified risk of severe IVH unless they have study.5,6 These varying suggested sonographer. Images of the brain are additional clinical risk factors. time frames can lead to different taken in the coronal plane with timing of studies in the extremely anterior to posterior views and in the sagittal plane with appropriate TIME OF IVH OCCURRENCE preterm infant. Because 4- to 6-week screening is sensitive for identifying angulation on the left and right.7,29 The overwhelming majority of IVH in PVL and term equivalent cranial Use of the posterior fontanelle may the preterm infant occurs within the ultrasound findings are associated allow more detailed assessment of – first 3 days of life.20 24 Of those, with adverse neurodevelopmental the periventricular white matter and approximately 50% of hemorrhages outcomes, we recommend screening occipital lobes. These views allow occur within the first 5 hours, and during both time periods. excellent visualization of approximately 70% occur within the supratentorial structures but limited first 24 hours of life. By 7 days, 95% of Sequential ultrasonography appears views of the posterior fossa and IVH will have occurred, with a small to have the best yield for identifying cerebellum. The cerebellum has been percentage appearing at 7 to 10 lesions associated with cerebral palsy. shown to be a frequent site of injury, days.21,22 In an analysis of infants In infants with cerebral palsy, almost with significant hemorrhage requiring neurosurgical intervention for one third were found to have PVL on occurring in as many as 9% of posthemorrhagic hydrocephalus, the ultrasonography performed after preterm infants with a diagnosis average age of IVH development was 2 4 weeks of age.26 Among 12 739 made by appropriately performed days, with ventriculomegaly apparent by preterm infants who were screened ultrasonography.30,31 For this reason, 3daysofage.24 In this study, at 4 weeks of age and again at near additional imaging through the temporizing neurosurgical procedures TEA, notably, 14% had cystic PVL that mastoid fontanelle is recommended. were performed 3 weeks after IVH was only visible on the early imaging In cases of limited cerebellar development. Thus, frequent follow-up and had resolved by the time of the hemorrhage, there was much better of significant IVH until resolution or later study.27 Subgroup analysis imaging sensitivity when mastoid stabilization will likely allow for early revealed that in infants born at ,26 views were obtained (86%) than determination of ventricular dilation weeks’ gestation, 18.5% of PVL cases when only the anterior fontanelle was and the potential need for therapy. were missed by a single assessed (16%).32 However, mastoid ultrasonographic examination views are unable to detect cerebellar performed at TEA. However, a follow- microhemorrhages, which can only be REPEAT BRAIN IMAGING up study demonstrated that infants visualized with MRI. Apart from PVL may initially be observed during who had cystic PVL at any time on hemorrhage, cerebellar hypoplasia is the first week of life in the VLBW ultrasonographic imaging had also associated with motor and

Downloaded from www.aappublications.org/news by guest on October 2, 2021 PEDIATRICS Volume 146, number 5, November 2020 3 TABLE 1 Neuroimaging the Preterm Infant Modality Clinical Notes Timing Cranial ultrasonography Routine anterior and mastoid fontanelle, optional posterior fontanelle, 1. Initial scan within 7 d of age and vascular images 2. Repeat scan at 4–6 wk of age 3. Scan near term or discharge MRI Ideally nonsedated Optional, based on physician-family discussion; TEA CT Should be avoided in most instances — Preterm infants #30 wk or .30 wk with significant risk factors (see text). —, not applicable.

cognitive deficits.31 Although most sedating medications.35,36 Protocols and the effects the results may have cases of cerebellar hypoplasia have that rely on feeding the infant 20 to on an individual family may not be been associated with cerebral white 30 minutes before the scan and predictable.42,43 matter injury, other factors, including swaddling to limit movement have genetic and neurodegenerative generally been successful in avoiding syndromes, medications, infarction, significant sedation in the majority of RECOMMENDATIONS (TABLE 1) and nutrition, play a role in cerebellar cases. With the use of nonsedated • Infants born at a gestational age of growth and affect neurologic MRIs and the increasing availability of #30 weeks and selected infants outcomes. Thus, cerebellar imaging MRI-compatible equipment, this with a gestational age of may have important diagnostic and imaging has become more readily .30 weeks who are believed to be prognostic value as part of the obtainable. Yet, controversy persists at increased risk for brain injury on screening ultrasonographic regarding which infants should the basis of identified risk factors examination. The addition of high- receive MRI studies at TEA. Abnormal are recommended to be screened resolution linear color Doppler findings on MRIs performed at TEA in for IVH with appropriately images obtained through the anterior a group of infants born at ,30 weeks’ performed cranial ultrasonography. fontanelle can be used to evaluate for gestation have been shown to be These risk factors may include, but patency of the superior sagittal sinus. predictive of psychomotor delay and are not limited to, placental If there is concern for venous sinus cerebral palsy at 2 years of age.37 The abruption, need for vigorous thrombosis, the posterior and predictive value of MRI at TEA for resuscitation, hypotension mastoid windows can additionally school-aged neurocognitive outcomes requiring pressor support, severe help to evaluate the sagittal and is less clear. One study reported that acidosis, prolonged mechanical transverse sinuses. Many centers are abnormal brain MRI at TEA was ventilation, confirmed sepsis, or also measuring the resistive index of predictive of adverse pneumothorax. the anterior cerebral artery as neurodevelopmental outcomes at • a marker for vascular compliance and 7 years of age.38 This association with Routine cranial ultrasonographic to document normal waveforms and adverse neurodevelopmental screening is recommended by 7 to diastolic flow. outcome at 7 years of age was 10 days of age for infants born at # ’ particularly striking for abnormalities 30 weeks gestational age. in the white matter, deep gray matter, Screening before 7 days of age may MRI and cerebellum. However, other be indicated for infants with MRI has become increasingly popular studies have reported39,40 that adding clinical signs and symptoms fi as a means of identifying brain injury MRI to early and late cranial suggestive of signi cant brain in the preterm infant. MRI provides ultrasonography did not improve injury. Repeat cranial the most detailed imaging of the brain prediction of severe intellectual ultrasonographic screening is and avoids the radiation risks disability or neurodevelopmental recommended to be performed associated with CT.33 Specific impairment at 6 to 7 years of age. at 4 to 6 weeks of age and at absorption rates (a measure of power Obtaining routine MRI has also not TEA or before hospital of radiofrequency fields) in patients been shown to have a clinically discharge. undergoing magnetic resonance significant effect on maternal anxiety • Infants with abnormal cranial procedures appear to be much lower or improve quality of life, although it ultrasonography findings are in neonates than adults and within may increase the cost of care.41 As the recommended to have repeat serial a safe and acceptable range.34 MRI Choosing Wisely9 campaign cranial ultrasonography as studies may be successfully identified, there is insufficient clinically indicated on the basis of performed in the preterm population evidence that routine brain MRI at chronological as well as at TEA without the use of any TEA improves long-term outcomes, gestational age.

Downloaded from www.aappublications.org/news by guest on October 2, 2021 4 FROM THE AMERICAN ACADEMY OF PEDIATRICS • Standard cranial ultrasonographic Susan Wright Aucott, MD, FAAP LIAISON Jay P. Goldsmith, MD, FAAP screening includes views from the Manuel A. Viamonte, MD – Section on Ivan L. Hand, MD, FAAP anterior and mastoid fontanelles. Pediatric Trainees David Alan Kaufman, MD, FAAP Additional posterior fontanelle and Camilia Rivera Martin, MD, FAAP vascular imaging can be performed Karen M. Puopolo, MD, PhD, FAAP STAFF for additional information. Paul Spire • CT is no longer considered a part of routine imaging techniques of the LIAISONS SECTION ON RADIOLOGY EXECUTIVE preterm brain. RADM Wanda D. Barfield, MD, MPH, FAAP – COMMITTEE, 2019–2020 • On the basis of available evidence, Centers for Disease Control and Prevention Sarah S. Milla, MD, FAAP, Chairperson MRI for infants born at ,30 weeks’ Lisa Grisham, MS, NP – National Association of Neonatal Nurses Adina L. Alazraki, MD, FAAP gestational age is not indicated as Tim Jancelewicz, MD – Section on Surgery Aparna Annam, DO, FAAP a routine procedure. MRI may be Russell Miller, MD – American College of Ellen Benya, MD, FAAP offered at TEA to the high-risk Obstetricians and Gynecologists Brandon P. Brown, MD, MA, FAAP infant after a conversation with the Meredith Mowitz, MD, MS, FAAP – Section on Hansel J. Otero, MD, FAAP Edward Richer, MD, FAAP family regarding the limitations of Neonatal-Perinatal Medicine Michael R. Narvey, MD, FAAP – Canadian this test for estimation of long-term Paediatric Society STAFF prognosis. When possible, it is recommended that the brain MRI Laura Laskosz, MPH be performed without contrast in STAFF the nonsedated state by using a “feed and wrap” technique. Jim Couto, MA ABBREVIATIONS AAN: American Academy of LEAD AUTHORS Neurology SECTION ON NEUROLOGY EXECUTIVE Ivan L. Hand, MD, FAAP CT: computerized tomography COMMITTEE, 2019–2020 Renée A. Shellhaas, MD, MS, FAAP IVH: intraventricular hemorrhage Sarah S. Milla, MD, FAAP Adam L. Hartman, MD, FAAP, Chairperson PVHI: periventricular hemorrhagic Josh L. Bonkowsky, MD, PhD, FAAP infarct COMMITTEE ON FETUS AND NEWBORN, Jamie K. Capal, MD, FAAP PVL: periventricular leukomalacia Timothy E. Lotze, MD, FAAP 2019–2020 Renée A. Shellhaas, MD, FAAP TEA: term equivalent age James J. Cummings, MD, FAAP, Chairperson David K. Urion, MD VLBW: very low birth weight Ira S. Adams-Chapman, MD, FAAP

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2020 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: No external funding. POTENTIAL CONFLICT OF INTEREST: The 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 October 2, 2021 PEDIATRICS Volume 146, number 5, November 2020 7 Routine Neuroimaging of the Preterm Brain Ivan L. Hand, Renée A. Shellhaas, Sarah S. Milla and COMMITTEE ON FETUS AND NEWBORN, SECTION ON NEUROLOGY, SECTION ON RADIOLOGY Pediatrics originally published online October 26, 2020;

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Downloaded from www.aappublications.org/news by guest on October 2, 2021 Routine Neuroimaging of the Preterm Brain Ivan L. Hand, Renée A. Shellhaas, Sarah S. Milla and COMMITTEE ON FETUS AND NEWBORN, SECTION ON NEUROLOGY, SECTION ON RADIOLOGY Pediatrics originally published online October 26, 2020;

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