By Gardner, Marcia R
Germinal matrix-intraventricular hemorrhage, periventricular hemorrhagic infarction, and periventricular leukomalacia are common brain injuries in preterm infants that can have significant long- term influences on children’s development, physical skills, and cognitive functioning. Characteristics of preterm infants, including immature cerebrovascular autoregulation, fragility of blood vessels, and the presence of the germinal matrix, increase their vulnerability to neurologic injury. Grades I-II germinal matrix- intraventricular hemorrhage tends to have little-to-moderate long- term impact on cognitive and neuromotor development after the neonatal period, while more severe hemorrhage is associated with less optimistic developmental prognoses. Periventricular leukomalacia and ventriculomegaly in the neonate are associated with severe cognitive disabilities as well as with cerebral palsy. Neurodevelopmental strategies emerging from both the neonatal developmental care and early intervention models may have a place in the post-acute care of newborns who experienced these insults. Vigilant developmental screening and early developmental intervention are essential components of the follow-up nursing care for children whose medical histories include neonatal brain injury.
Children who experience non-transient neurological insults during the perinatal and neonatal period constitute an important group in pediatric nursing because they have significant health needs and consume many health and educational resources (Chan et al., 2001; Hack et al., 1994). The majority of children who experience perinatal/neonatal neurologic insults are born preterm (Volpe, 2001), and many are extremely low birth weight, extremely preterm infants (Fanaroff et al., 1995). See Table 1 for definitions commonly associated with gestational age and birthweight. A range of chronic and disabling conditions, including cognitive impairment, learning disabilities, psychiatric disorders, functional disabilities, sensory impairment, and mobility disorders are associated with the particular neonatal neurologic insults of intraventricular hemorrhage, ventriculomegaly, and periventricular parenchymal damage (Aziz et al., 1995; Hack et al., 1994; Jakobson, Frisk, Knight, Downie, & Whyte, 2001; Resnick et al., 1998; Volpe, 1998). As neonatal intensive care units continue to expand the boundaries of gestational age and birth weight survival (McCormick, 1997), nurses and other health care professionals may be caring for larger numbers of children with this history and with similar complex health conditions.
Physiologic Context for Outcomes
Childhood outcomes vary according to the severity and type of neonatal brain injury. These are briefly reviewed below to provide context for understanding outcomes in children who experience intracranial hemorrhage and/or brain parenchymal injury.
Intracranial hemorrhage. Intracranial hemorrhage (ICH) occurs in both term and preterm infants, although causative factors in these neonatal groups differ. ICH in the term infant is primarily a function of birth trauma, while ICH in the preterm infant can be trauma-related but is often a function of neurological and vascular immaturity. The majority of cases of neonatal ICH are seen in the preterm population, primarily because of obstetrical and neonatal clinical advances that have minimized birth trauma in term infants and have improved survival rates of low birth weight and preterm infants (Vohr et al., 2000; Volpe, 1998, 2001). Germinal matrix intracranial hemorrhage (GM-IVH) is both the most frequent neonatal ICH and the hallmark ICH of the preterm infant. Bleeding is believed to be a result of blood vessel fragility in the germinal matrix in combination with poor cerebral autoregulation, and the risk for GM- IVH decreases significantly after 32 weeks of gestation (Annibale & Hall, 2003).
The severity of intraventricular-periventricular hemorrhage (IVH- PVH) is determined by the presence of blood in the germinal matrix and ventricles demonstrated by cranial ultrasound scan. Table 2 summarizes the classic ultrasound grading scheme for IVH-PVH (Annibale & Hill, 2003; Papile, Burstein, Burstein, & Koffler, 1978; Perlman & Rollins, 2000). Grade IV hemorrhage is most severe and reflects hemorrhage into the brain parenchyma.
ICH rates are somewhat variable among neonatal centers, and are related to birth weight and gestational age of infants, as well as to population characteristics and treatment modes (Clark, Dykes, Bachman, & Ashurst, 1996; Synnes et al., 2001). A 1995 study found that about 34% of very low birthweight infants between 501 and 1,500 grams had experienced any ICH, and up to 18% had ICH findings of grade III and higher (Fanaroff et al., 1995); a recent review estimated the incidence of GM-IVH in very low birthweight infants to be around 20% (Roland & Hill, 2003). Smaller and less mature infants consistently demonstrate higher rates and severity of ICH (Vohr et al., 2000). Approximately 5 to 10% of infants with ICH will develop hydrocephalus, potentially resulting in further neuron degeneration, and in the need for surgical intervention and potential pulmonary, infection, and other complications (Chumas, Tyagi, & Livingston, 2001; Heep, Engelskirchen, Holschneider, & Groneck, 2001). Neurodevelopmental outcomes of infants needing surgical interventions, such as ventriculostomy and placement of ventricular shunts, are related to the severity of hemorrhage and resultant brain injury rather than to shunting or complications of surgery (Reinprecht et al., 2001). Ventriculomegaly without increased intracranial pressure is also associated with ICH. especially in infants with grades III and IV IVH-PVH, and ventriculomegaly is also a predictor of impaired developmental progress (Ment et al., 1999).
Table 1. Definitions Related to Birthweight and Age Used in Cited Neonatal Outcomes Studies
Strategies to prevent ICH. Prophylactic medications have shown promise for the prevention of grades III and IV hemorrhage in low birth weight, preterm infants. Both antenatal steroid administration and postnatal indomethacin administration have been evaluated (Fowlie, 1996: Ment et al., 1994; Ment et al., 1995). The mechanism by which these medications act to prevent IVH-PVH is unclear, although both agents appear to have blood vessel maturing and stabilizing effects (Ment et al., 1994; Ment et al., 1995), and indomethacin is known to mediate cerebral blood flow and prostaglandin function (Volpe, 1994). However, although a protective effect of indomethacin has been shown, studies are equivocal regarding its relationship to long-term neurodevelopmental functioning in these infants (Ment et al., 1994: Ment et al., 2004; Schmidt et al., 2001). Antenatal steroids have also demonstrated consistent effects for preventing IVH-PVH (Sehdev et al., 2004; Volpe, 2001). Yet, the main strategy for prevention of IVH-PVH continues to be atraumatic delivery of the infant and effective post- delivery regulation of physiologic status, especially oxygen and fluid status, in an effort to minimize deleterious changes in cerebral perfusion, vessel pressures, and oxygenation (Annibale & Hill. 2003).
Periventricular parenchymal damage. Periventricular hemorrhagic infarction (PHI) and periventricular leukomalacia (PVL) are the most common and potentially disabling brain parenchymal disorders in newborns. Periventricular leukomalacia occurs more frequently in preterm than in term infants, and periventricular hemorrhagic infarction is seen almost exclusively in preterm infants (Volpe, 1998, 2001). In the preterm population, PHI is seen in association with GM-IVH, and is characterized by hemorrhagic and necrotic damage to cerebral white matter (Volpe, 1998).
PVL in the preterm infant is associated with several perinatal and neonatal risk factors, including premature rupture of membranes, maternal chorioamnionitis, asphyxia, and GM-IVH (De Felice et al., 2001; Wu & Colford, 2000). PVL is characterized by severe focal and less severe diffuse cerebral white matter injury, including destruction of neurons in the periventricular white matter, diffuse destruction of oligodendrocytes, impaired myelination, decreased total cerebral white matter, and ventriculomegaly (Volpe, 2001). Over time, damaged areas of the brain evolve as cysts visible on ultrasound scan (Pierrat et al., 2001). Cystic PVL is a predictor of cerebral palsy (CP) (Dunin-Wasowics et al., 2000; Pinto-Martin et al., 1995: Wu & Colford. 2000).
Post-insult Outcomes
GM-IVH in the preterm neonate can result in damage to the neural precursor cells residing in the fetal germinal matrix, so long-term effects of ICH may be related to both immediate damage as well as inhibition of appropriate functioning of neural cells derived from the germinal matrix (Raz et al., 1994). Periventricular hemorrhagic infarction and periventricular leukomalacia involve both local and more diffuse permanent cerebral white matter injury (Volpe, 1998, 2001). Such neurologic insults can both profoundly and subtly influence children’s developmental trajectories and functioning over time. How and when the clinical manifestations of these insults become apparent depends on the severity and type of brain injury.
Early Developme\ntal Outcomes
Infants through preschoolers. Extremely low birthweight, extremely premature infants represent the population at greatest risk for GM-IVH and PVL (Volpe, 1998, 2001). Within this sub- population of preterm infants, one study found that approximately half of the sample had a neuromotor disability, and 10 to 20% manifested a severe developmental or other disability associated with neonatal brain injury by 30 months corrected age (Wood, Marlow, Costeloe, Gibson, & Wilkinson, 2000). In this population, complex parenchymal brain injury involving PHI and PVL is recognized as a significant predictor of severe developmental delay (Volpe 1998, 2001), commonly measured with standard infant developmental scales such as the Bayley Scales of Infant Development Mental Development Index (BSID-AADI) (Bayley, 1969), the Wechsler Intelligence Scales for Children (WISC) (Wechsler, 1991), and the Vineland Adaptive Behavior Scales (VABS) (Sparrow, Balla, & Cicchetti, 1984), among others.
Early developmental outcomes associated with less severe injury are more reassuring. In one study, developmental outcomes of LBW preterm infants with transient, low-grade (I-II) ICH ultrasound findings were similar to outcomes in infants without a history of any brain injury at age 1 year (Whitaker et al.,1990).
Hack et al. (2000) found 53% of a sample of 221 ELBW infants with Grade III or higher IVH had severe developmental delays at age 20 months, and 69% had some form of developmental impairment, defined as any cognitive, motor, or sensory problem. In this same study, 56% of infants with ventriculomegaly had severe delays, and 71% had any impairment; 63% of infants with PVL had severe delays, and 75% overall had an impairment. Additional studies have shown similar significant relationships among the lowest birthweights, lowest gestational ages, and complex brain injury, and between complex brain injury and significant neurodevelopmental impairments including cognitive and motor delays as well as cerebral palsy manifesting from infancy through preschool ages (Ment et al., 1999; Pierrat, 2001).
Specifically, in one of these studies, 74% of infants with PVL associated with small, localized cystic changes had signs of cerebral palsy by 24 months corrected age. Of the infants with extensive cystic PVL who survived past 40 weeks corrected age, 96% had signs of cerebral palsy by 24 months corrected age, and of these, less than 1% could walk independently by age 5 years (Pierrat, 2001). Table 3 summarizes additional details of studies of developmental outcomes from infancy through preschool age.
Later Developmental Outcomes
School-aged children. Developmental outcomes for school-aged children who experienced severe IVH in the neonatal period are similar to those for younger children with severe IVH – the more severe the IVH, the more severe the developmental impact and the higher the risk for severe mental retardation and cerebral palsy. The most sensitive predictors of sensory, cognitive, language, psychomotor, and academic functioning in early school-aged children, as in younger children, are birth weight and gestational age combined with cranial ultrasound findings (Hack et al., 1994).
Table 3. Developmental Outcomes in Infants, Toddlers, and Preschoolers
A study of 685 low birthweight 6-year-olds found that children whose cranial ultrasound scans in the neonatal period showed ventricular enlargement or parenchymal lesions had significantly higher risks of mental retardation and borderline intelligence than those without these lesions. Children whose ultrasound scans showed GM-IVH only were also at some increased risk for mental retardation and borderline intelligence (Whitaker et al., 1996). The group of children who had neonatal cranial ultrasound findings consistent with ventricular enlargement or parenchymal damage had a significantly higher prevalence of attention deficit-hyperactivity disorder (ADHD), tic disorder, and all psychiatric disorders than those without cranial ultrasound abnormalities or with only GM-IVH. Children with no cranial ultrasound abnormalities and those with a history of GM-IVH only did not differ relative to the prevalence of psychiatric disorders (Whitaker et al., 1997).
In this same sample, children of normal intelligence with ventricular enlargement or parenchymal lesions demonstrated poorer visual perceptual organization than did a comparison group without ultrasound abnormalities (Whitaker et al., 1996). Jakobson et al. (2001) also documented the relationship between the severity of IVH and/or PVL and increased visual perceptual deficits in a group of 6- year-olds born preterm with ELBW. Table 4 summarizes details of studies of developmental outcomes in school-aged children.
Overall, the presence of IVH on cranial ultrasound is a strong predictor of utilization of special education services (Resnick et al., 1998). Approximately 30% of children with any IVH have eligibility for special education services and demonstrate poorer school achievement than children without these Findings (Boyce, Smith, & Casto, 1999). Furthermore, in a recent study of adolescents born at 32 weeks gestation or younger, IVH-PVH was also strongly predictive of poor school performance and use of special education services (van de Bor & den Ouden, 2004). Overall, the severity of IVH is consistently related to greater developmental delay at preschool and school-age time points (Bendersky & Lewis, 1995; Boyce et al., 1999).
Table 4. Developmental Outcomes in School-aged and Adolescent Children
Summary of Clinical Outcomes
Extremely low birth weight, extremely preterm infants are at the greatest risk of all neonates for GMIVH, PHI, and PVL insults that can result in severely impaired neurodevelopment and cognitive functioning (Volpe, 1998). Children who had simple GM-IVH (grades I- II) tend to have less severe impairments than those who developed parenchymal lesions or ventriculomegaly as neonates (Hack et al., 2000; Whitaker et al., 1996). Some children who had GM-IVH have little or no developmental sequelae during infancy and early childhood (Whitaker et al., 1990), although it is possible that some developmental outcomes of grades I-H GM-IVH are so subtle that they are not identified on standard scales. In addition, other studies suggest that a variety of related impairments emerge later in the developmental trajectory (Boyce et al., 1999; Whitaker et al., 1996), and that cognitive problems persist at least through early adolescence. Children who as infants were found to have more extensive IVH (grade III or higher) are likely to demonstrate severe developmental delays during infancy and early childhood, and to demonstrate severe cognitive and perceptual disorders later.
Ventriculomegaly and PVL correlates found on cranial ultrasound in neonates are associated with severe developmental and motor delays, including disorders of muscle tone and clinically diagnosed cerebral palsy (Hack et al., 2000; Ment et al., 1999; Pinto-Martin et al., 1995; Whitaker et al., 1996). Increasing severity of PVL is associated with more severe neurologic abnormalities (Pierrat et al., 2001). Parenchymal brain injury is also associated with behaviors consistent with attention deficit-hyperactivity disorder and with other psychiatric syndromes in young school-aged children (Whitaker et al., 1997).
Nursing Issues for Mediating The Impact of Neonatal Brain Injury
The profound long-term effects of severe neonatal brain injury include cognitive, physical, and behavioral disabilities that ultimately stress parent, family, educational, and societal resources. If risks for neonatal neurologic injuries can be minimized, long-term outcomes should be reduced in frequency and severity as well. For infants who have already experienced neurologic insults, nurses can incorporate strategies for developmental enhancement and early detection of disabilities into assessment and care.
Developmental enhancement. Targeted developmental strategies that decrease environmental stressors and increase environmental supports (for example, “developmental care”) have been effective for improving physiological stability, increasing the rate of weight gain, and improving neurobehavioral outcomes in low-risk preterm infants without medical complications (Als et al., 1994; Buehler, Als, Duffy, McAnulty, & Liederman, 1995; Westrup, Kleberg, von Eichwald, Stjernqvist, & Lagercrantz, 2000). In addition, structured multisensory interventions, including auditory stimulation with a female voice, eye contact, stroking, and rocking, improved alertness in stable preterm infants with PVL, and improved oral nipple feedings promoted faster progression to discharge in preterm infants with IVH and/or PVL (White-Traut et al., 1999; White-Traut et al., 2002). Multisensory stimulation continuing to 2 months of age (corrected) resulted in a trend toward better neurodevelopmental status at one year of age, although infants with PVL had significantly worse mental development scores overall than those with simpler injury (Nelson et al., 2001). There is limited additional data on the use of developmental strategies specifically with brain-injured neonates during the convalescent period.
Interdisciplinary care. An interdisciplinary approach to care during hospital convalescence is essential for ensuring that functional status is maximized and for promoting the best possible discharge status for the infant. Nursing participation in the development and implementation of the interdisciplinary strategies and plan of care will ensure that all relevant information about infant status is incorporated, and that recommended interventions are implemented consistently. Parents should be educated about common behaviors and developmental needs of preterm infants and can be assisted to learn developmental care strategies, such as targeted stimulation, positioning, interaction, and fee\ding skills based on individual infant characteristics. Also, nurses are instrumental in reinforcing parents’ use of other therapeutic strategies recommended by the interdisciplinary team, and in helping them appreciate the progress that their infants have made. Families should be referred as appropriate to community-based resources including early intervention and home care programs.
Childhood screening. After the neonatal period, children who have experienced severe IVH or who have ventriculomegaly or periventricular leukomalacia will present with significant developmental delays during infancy. In addition to providing information and empathetic support, nurses can help families by referring these infants, even before disabilities are obvious, for developmental follow-up and multidisciplinary interventional therapies including community early intervention programs. Children who have medical histories that include simple GM-IVH should be screened carefully for subtle developmental, behavioral, or perceptual problems, as their impairments may manifest later and may not be as clear-cut or as obvious as those with more severe brain injuries. It is important to continue intensive developmental screening throughout childhood, as a range of perceptual, auditory, learning, or behavioral-psychiatric disabilities may develop later, even when infant and toddler developmental screens appear essentially normal. These more subtle disabilities can have a very significant effect on children’s social and school functioning. Children with these subtle challenges generally require special educational services and multi-disciplinary supports as well (Flanagan, Jackson, & Hill, 2003; Specht, 2004).
Outcomes research on infants who experienced neurologic insults at or after birth illustrates the vulnerability of the brain to injury and the lasting impact of this injury on function, behavior, and learning. These infants and children, especially those with the most severe sequelae of ICH and periventricular parenchymal damage, require large and potentially costly investments of time and resources in health care and education settings, as well as emotional investment from parents, caregivers, educators, and health professionals; the “costs” of these psychological investments are much more difficult to calculate. Any interventions that can reduce the degree of disability affecting these infants as they grow theoretically also should reduce burdens on families and society. Many of these infants will receive developmental interventions post- discharge through community early intervention programs, but it is unclear what role the consistent initiation of targeted developmental care prior to hospital discharge plays in reducing long-term disability and enhancing long-term cognitive, motor, and functional performance. In the short term, multisensory stimulation can promote behaviors necessary for functional adaptation in brain- injured preterm infants and can reduce the costs of neonatal care through earlier discharge to home (White-Traut, et al., 2002). More research in this area of nursing care is needed.
Conclusion
Children who previously received developmentally supportive care along the developmental care model (Als et al., 1994) during the neonatal period are reaching the ages for long-term developmental follow-up. Data should begin to be available to evaluate whether this model of care influences dimensions of childhood development in low-risk preterm infants. Extending this model by evaluating the long-term impact of basic developmental interventions on infants with IVH, PVL, and other neonatal brain injuries will provide additional information about the influence of predischarge nursing care on later developmental functioning. The use of an interdisciplinary approach to care, vigilant screening of children with a history of neonatal brain injury, parent education, and referral to appropriate services are important nursing strategies for identifying problems and initiating comprehensive programs of intervention.
References
Als, H., Lawhon, G., Duffy, F.H., McAnulty, G.B., Gibes- Grossman, R., & Buckman, J.G. (1994). Individualized developmental care for the very lowbirth-weight preterm infant: medical and neurofunctional effects. Journal of the American Medical Association, 272(11), 853-858.
Annibale, D.J., & Hill, J. (2003). Periventricular hemorrhage- intraventricular hemorrhage. Retrieved February 20, 2005, from http:/ /www.emedicine.com/ped/topic 2595.htm
Aziz, K., Vickar, D.B., Suave, R.S., Etches, P.C., Pain, K.S., & Robertson, C.M. (1995). Province-based study of neurologic disability of children weighing 500-1249 grams at birth in relation to neonatal cranial ultrasound findings. Pediatrics, 95(6), 837- 844.
Bayley, N. (1969). Manual for the Bayley Scales of Infant Development. Cleveland, OH: Psychological Association.
Bendersky, M., & Lewis, M. (1995). Effects of intraventricular hemorrhage and other medical and environmental risks on multiple outcomes at age three years. Journal of Developmental and Behavioral Pediatrics, 16(2), 89-96.
Boyce, G.C., Smith, T.B., & Casto, G. (1999). Health and educational outcomes of children who experienced severe neonatal medical complications. Journal of Genetic Psychology, 160(3), 261- 269.
Buehler, D.M., Als, H., Duffy, F.H., McAnulty, G.B., & Liederman, J. (1995). Effectiveness of individualized developmental care for low-risk preterm infants: Behavioral and electrophysiologic evidence. Pediatrics, 96(5), 923-932.
Chan, K., Ohlsson, A., Synnes, A., Lee, D., Chien, L., & Lee, S.K. (2001). Survival, morbidity, and resource use of infants of 25 weeks’ gestational age or less. American Journal of Obstetrics and Gynecology, 185(1), 220-226.
Chumas, P., Tyagi, A., & Livingston, J. (2001). Hydrocephalus What’s new? Archives of Disease in Childhood Fetal and Neonatal Edition, 85(3), F149-F154.
Clark, R.H., Dykes, F.D., Bachman, T.E., & Ashurst, J.T. (1996). Intraventricular hemorrhage and high-frequency ventilation: A meta- analysis of prospective clinical trials. Pediatrics, 98(6, Part 1 of 2), 1058-1061.
De Felice, C., Toti, P., Laurini, R.N., Stumpo, M., Picciolini, E., Todros, T., et al. (2001). Early neonatal brain injury in histologic chorioamnionitis. Journal of Pediatrics, 138(1), 101- 104.
Dunin-Wasowics, D., Rowecka-Trzeicka, B., Milewska-Bobula, B., KassurSiemienska, B., Auuer, A., Idzik, M., et al. (2000). Risk factors for cerebral palsy in very low-birthweight infants in the 1980s and 1990s. Journal of Child Neurology, 15(6), 417-420.
Fanaroff, A.A., Wright, L.L., Stevenson, K.D., Shankaran, S., Donovan, E.F., Ehrenkranz, R.A., et al. (1995). Very-low-birth- weight outcomes of the National Institute of Child Health and Human Development Neonatal Research Network, May 1991 December 1992. American Journal of Obstetrics and Gynecology, 773(5), 1423-1431.
Flanagan, N.M., Jackson, A.J., & Hill, A.E. (2003). Visual impairment in childhood: Insights from a community-based survey. Child, Health & Development, 29(6), 493-499.
Fowlie, P.W. (1996). Prophylactic indomethacin: Systematic review and meta-analysis. Archives of Disease in Childhood, 74, F81-F87.
Hack, M., Taylor, H.G., Klein, N., Eiben, R., Schatschneider, C., & Mercuri-Minich, N. (1994). School-age outcomes in children with birth weights under 750 g. New England Journal of Medicine, 331(12), 753-759.
Hack, M., Wilson-Costello, D., Friedman, H., Taylor, H.G., Schlucter, M., & Fanaroff, A.A. (2000). Neurodevelopment and predictors of outcomes of children with birth weights of less than 1000 g: 1992-1995. Archives of Pediatrics & Adolescent Medicine, 154(7), 725-731.
Heep, A., Engelskirchen, R., Holschneider, A., & Groneck, P. (2001). Primary intervention for posthemorrhagic hydrocephalus in very low birth-weight infants by ventriculostomy. Child’s Nervous System, 77, 47-51.
Jakobson, L.S., Frisk, V., Knight, R.M., Downie. A.L.S., & Whyte, H. (2001). The relationship between periventricular brain injury and deficits in visual processing among extremely-low-birthweight (
McCormick, M.C. (1997). The outcomes of very low birth weight infants: Are we asking the right questions? Pediatrics, 99(6), 869- 876.
Ment, L.R., Oh, W., Ehrenkranz, R.A., Philip, A.G., Duncan, C.C., & Makuch, R.W. (1995). Antenatal steroids, delivery mode, and intraventricular hemorrhage in preterm infants. American Journal of Obstetrics and Gynecology, 172(3), 795-800.
Ment, L.R., Oh, W., Ehrenkranz, R.A., Philip, A.G., Vohr, B.R., Allan, W., et al. (1994). Low-dose indomethacin and prevention of intraventricular hemorrhage: A multicenter randomized trial. Pediatrics, 93(4), 543-550.
Ment, L.R., Vohr, B.R., Allan, W., Westerveld, M., Katz, K.H., Schneider, K.C., et al. (1999). The etiology and outcome of cerebral ventriculomegaly at term in very low birth weight preterm infants. Pediatrics, 104(2, Parts 1 & 2), 243-248.
Ment, L.R., Vohr, B.R., Makuch, R.W., Westerveld, M., Katz, K.H., Schneider, K.C., et al., (2004). Prevention of intraventricular hemorrhage by indomethacin in male preterm infants. Journal of Pediatrics, 145, 832-834.
Nelson, M.N., White-Traut, R.C., Vasan, U., Silvestri, J., Comiskey, E., Meleedy-Rey, P., et al., (2001). One-year outcome of auditory-tactile-visual-vestibular intervention in the neonatal intensive care unit: effects of severe prematurity and central nervous system injury. Journal of Child Neurology, 16(7), 493-498.
Papile, L., Burstein, J., Burstein, R., & Koffler, H. (1978). Incidence and evolution of subependymal and intraventricular hemorrhage: A study of infants with birth weights less than 1500 grams. Journal of Pediatrics, 92, 529-534
Perlman, J.M., & Rollins, N. (2000). Surveillance protocol for the detection of intracranial abnormalities in premature neonates. Archives of Pediatrics and Adolescent Medicine, 154(8). 822-826\.
Pierrat, V., Duquennoy, C., van Haastert, I.C., Ernst, M., Guilley, N., & de Vries, L.S. (2001). Ultrasound diagnosis and neurodevelopmental outcome of localised and extensive cystic periventricular leucomalacia. Archives of Disease in Childhood Fetal and Neonatal Edition, 84(3). F151-F156.
Pinto-Martin, J.A., Riolo, S., Cnaan, A., Holzman, C., Susser, M.W., & Paneth, N. (1995). Cranial ultrasound prediction of disabling and nondisabling cerebral palsy at age two in a low birthweight population. Pediatrics, 95(2), 249 254.
Raz, S., Foster, M.S., Briggs, S.D., Shah, F., Baertschi, J.C., Lauterbach, M.D., et al. (1994). Lateralization of perinatal cerebral insult and cognitive asymmetry: Evidence from neuroimaging. Neuropsychology, 8(2), 160-170.
Reinprecht, A., Dietrich, W., Berger, A., Bavinzski, G., Weninger, M., & Czech, T. (2001). Posthemorrhagic hydrocephalus in preterm infants: Long-term follow-up and shunt-related complications. Child’s Nervous System, 17(11), 663-669.
Resnick, M.B., Gomatam, S.V., Carter, R.L., Ariet, M., Roth, J., Kilgore, K.L., et al. (1998). Educational disabilities of neonatal intensive care graduates. Pediatrics, 102(2, Part 1 of 3), 308-314.
Roland, E.H., & Hill, A. (2003). Germinal matrix- intraventricular hemorrhage in the premature newborn: Management and outcome. Neurologic Clinics of North America, 21, 833-851.
Schmidt, B., Davis, P., Moddemann, D., Ohlsson, A., Roberts, R., Saigal, S., et al. (2001). Long-term effects of indomethacin prophylaxis in extremely-low-birthweight infants. New England Journal of Medicine, 344(26), 1966-1972.
Sehdev, H., Abbasi, S., Robertson, P., Fisher, L., Marchiano, D., Gerdes, J. & Ludmir, J. (2004). The effects of the time interval from antenatal corticosteroid exposure to delivery on neonatal outcome of very low birthweight infants. American Journal of Obstetrics and Gynecology, 191, 1409-1413.
Sparrow, S. Balla, D., & Cicchetti, D.V. (1984). Vineland Adaptive Behavior Scales. Circle Pines, MN: AGS/American Guidance Service.
Specht, J. (2004). Educating exceptional children: Current issues for educators. Education Canada, 44(1), 4-7.
Synnes, A., Chien, L., Peliowski, A., Baboolal, R., Lee, S.K., & Network, C.N. (2001). Variations in intraventricular hemorrhage incidence rates among Canadian neonatal intensive care units. Journal of Pediatrics, 138(4), 525-531.
van de Bor, M., & den Ouden, L. (2004). School performance in adolescents with and without periventricular-intraventricular hemorrhage in the neonatal period. Seminars in Perinatology, 28(4), 295-303.
Vohr, B.R., Wright, L.L., Dusick, A.M., Mele, L., Verier, J., Steichen, J.J., et al. (2000). Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993-1994. Pediatrics, 105(6), 1216-1226.
Volpe, J.J. (1994). Brain injury caused by intraventricular hemorrhage: Is indomethacin the silver bullet for prevention? Pediatrics, 93(4), 673-677.
Volpe, J.J. (1998). Neurologic outcome of prematurity. Archives of Neurology, 55(3), 297-300.
Volpe, J.J. (2001). Neurology of the Newborn (4th ed.). Philadelphia: W.B. Saunders.
Wechsler, D. (1991). Wechsler Intelligence Scale for Children (3rd ed.). San Antonio, TX: Psychological Corporation.
Westrup, B., Kleberg, A., von Eichwald, K., Stjernqvist, K., & Lagercrantz, H. (2000). A randomized controlled trial to evaluate the effects of the newborn individualized developmental care and assessment program in a Swedish setting. Pediatrics, 105(1, Part 1 of 3), 66-72.
Whitaker, A.M., Feldman, J.F., Van Rossem, R., Schonfeld, I.S., Pinto-Martin, J.A., Torre, C., et al. (1996). Neonatal cranial ultrasound abnormalities in low birth weight infants: Relation to cognitive outcomes at six years of age. Pediatrics, 98(4, Part 1 of 2), 719-729.
Whitaker, A.M., Johnson, J., Sebris, S., Pinto, J., Wasserman, G., Kairam, R., et al. (1990). Neonatal cranial ultrasound abnormalities: association with developmental delay at age one in low birth weight infants. Developmental and Behavioral Pediatrics, 11(5), 253-260.
Whitaker, A.H., Van Rossem, R., Feldman, J.F., Schonfeld, I.S., Pinto-Martin, J.A., Torre, C., et al. (1997). Psychiatric outcomes in low-birth-weight children at age 6 years: Relation to neonatal cranial ultrasound abnormalities. Archives of General Psychiatry, 54(9), 847-856.
White-Traut, R.C., Nelson, M.N., Silvestri, J.M., Patel, M., Vasan, U., Man, B.K., et al. (1999). Developmental intervention for preterm infants diagnosed with periventricular leukomalacia. Research in Nursing and Health. 22, 131-143.
White-Traut, R.C., Nelson, M.N., Silvestri, J.M., Vasan, U., Littau, S., Meleedy-Rey, P., et al. (2002). Effect of auditory, tactile, visual, and vestibular intervention on length of stay, alertness, and feeding progression in preterm infants. Developmental Medicine and Child Neurology, 44, 91-97.
Wood, M.S., Marlow, N., Costeloe, K., Gibson, A.T., & Wilkinson, A.R. (2000). Neurologic and developmental disability after extremely preterm birth. New England Journal of Medicine, 343(6), 378-384.
Wu, Y.W., & Colford, J.M. (2000). Chorioamnionitis as a risk factor for cerebral palsy: A meta-analysis. Journal of the American Medical Association, 284(11), 1417-1424.
Marcia R. Gardner, MA, RN, CPNP, CPN, is Assistant Professor of Nursing, Drexel University, and doctoral candidate, University of Pennsylvania School of Nursing, both in Philadelphia, PA.
Acknowledgment: Part of this work was funded by NIH Grant 5T32NR07100-04: Research on Vulnerable Women, Children, and Families.
Copyright Anthony J. Jannetti, Inc. Nov/Dec 2005
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