Behavioral Problems and Socioemotional Competence at 18 to 22 Months of Extremely Premature Children
BACKGROUND: Behavior and socioemotional development are crucial aspects of child development .
METHODS: A total of 2505 children born at <27 weeks’ gestation was evaluated at 18 to 22 months’ corrected age between January 1, 2008 and December 12, 2012 (86% follow-up). The Brief Infant and Toddler Social and Emotional Assessment was used to evaluate behavioral and socioemotional problems. Cognition and language were evaluated by using the Bayley Scales of Infant and Toddler Development, Third Edition (Bayley-III). Logistic regression analysis was used to evaluate for perinatal and demographic factors associated with behavioral problems (≥75th percentile) and delayed socioemotional competence (≤15th percentile). Structural equation modeling with bootstrapping was used to identify possible associated risk factors and Bayley-III scores as mediators.
RESULTS: Thirty-five percent (873) of children had behavioral problems, and 26% (637) displayed deficits in socioemotional competence. Male sex, public insurance, mothers with less than a high school education, and lower maternal age were associated with behavioral problems. Deficits in competence were associated with lower birth weight, public insurance, mothers with less than a high school education, and abnormal neuromotor exam. Bayley-III language and cognitive scores were significant mediators of the relationships between risk factors and both behavioral and competence scores (P < .05).
CONCLUSIONS: Extremely premature children are at risk for behavioral problems and deficits in socioemotional competence. Sociodemographic factors were associated with both socioemotional competence and behavioral problems. Deficits in socioemotional competence were also associated with neuromotor abnormalities and cognitive and language function
- ASD —
- autism spectrum disorder
- Bayley-III —
- Bayley Scales of Infant and Toddler Development, Third Edition
- BITSEA —
- Brief Infant and Toddler Social and Emotional Assessment
- BPD —
- bronchopulmonary dysplasia
- BW —
- birth weight
- CA —
- corrected age
- CP —
- cerebral palsy
- ELBW —
- extremely low birth weight
- EP —
- extremely premature
- GA —
- gestational age
- HS —
- high school
- IVH —
- intraventricular hemorrhage
- NICHD —
- Eunice Kennedy Shriver National Institute of Child Health and Human Development
- NRN —
- Neonatal Research Network
What’s Known on This Subject:
Extremely premature children are at high risk for developmental problems. Behavior and socioemotional development are crucial aspects of child development.
What This Study Adds:
This study shows that extremely premature children are at risk for behavioral and socioemotional problems at an early age and that sociodemographic factors and neuromotor abnormalities are associated with these deficits. In addition, cognitive and language functioning mediates these deficits.
Extremely premature (EP) children are surviving more often and are at high risk for neurodevelopmental problems,1 although many survive free of neuromotor abnormalities.2 A substantial proportion of EP children have cognitive and behavioral problems even in the absence of detectable brain abnormalities on neuroimaging.3,4 Several factors may contribute to behavioral and socioemotional problems in EP children, including the vulnerability of the premature brain during critical periods of development,5,6 multiple medical problems,7 and the social and socioeconomic environment.8 Behavioral and socioemotional growth is a crucial aspect of child development. It influences cognition, motor function, and language, which have major impact on future school performance and overall functional outcomes.9,10 However, less is known about early behavioral and socioemotional development in EP children.11,12 Our previous research in 30-month-old corrected age (CA) formerly extremely low birth weight (ELBW) children showed that 46.8% of children had behavioral problems and 20.4% had deficits in socioemotional competence.13 Given the high rate of these problems evident by 30 months of age, determining if behavior and socioemotional problems are associated with early risk factors is imperative. Identification of early risk factors would enable practitioners to refer children at high risk earlier for behavioral intervention, thereby reducing the negative impact on children and families.14 In addition, a broader understanding is needed of the biological and social risk factors associated with poor behavioral or socioemotional outcomes in EP children.
The Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Neonatal Research Network (NRN) Follow-Up Program provides a unique opportunity to study behavioral and socioemotional competence problems in the EP population at an early age.
Our study aimed to estimate the rates of behavioral problems and deficits in socioemotional competence among EP children during their follow-up visit at 18 to 22 months’ CA. We hypothesized that EP children would have more behavioral problems and greater deficits in socioemotional competence when compared with norms. In addition, we sought to investigate factors associated with these difficulties, as well as mediating factors. This study provides new information concerning the prevalence of behavior and socioemotional problems before the age of 2 years in EP children, unique information concerning the relationship of neonatal and maternal factors to behavioral and socioemotional outcomes, as well as the mediating role of cognitive and language development by using Bayley Scales of Infant and Toddler Development, Third Edition (Bayley-III) scores.
The study population included all EP children <27 weeks’ gestation born without a major congenital abnormality in the NICHD NRN centers who had a standard follow-up visit at 18 to 22 months’ CA between January 1, 2008 and December 12, 2012 (Fig 1). A total of 5085 children met these criteria. Of these infants, 2187 died, 219 were lost to follow-up, and 90 had no follow-up status information. The remaining 2589 were evaluated at the follow-up visit, and 2505 children had complete data available, representing a follow-up rate of 86%. Those children included and not included did not differ significantly with respect to sex, race, necrotizing enterocolitis, intraventricular hemorrhage (IVH) grade 3 or 4, bronchopulmonary dysplasia (BPD), marital status, or gestational age (GA). There were more multiple births among the children included in the analysis (23% vs 16%; P < .01). They were less likely to have public insurance (72% vs 79%; P = .02) and fewer of them had mothers with less than a high school (HS) education (17% vs 24%; P < .01). Those in the analysis had mothers with a higher maternal age (27.4 ± 6.4 vs 26.6 ± 6.4; P = .03) and had a lower mean birth weight (BW) (765 ± 154 g vs 798 ± 198 g; P < .01).
Pregnancy, delivery, and hospitalization data were obtained prospectively by certified study coordinators until 120 days after birth or hospital discharge using standard definitions from the NRN. At the 18- to 22-month visit, interim medical history and updated social and demographic information were obtained from the parent or primary caregiver. Children underwent a standardized neurologic examination, including the administration of the modified Gross Motor Function Classification Scale,16 a scale that is scored from 0 (normal walking) to 5 (lower function); cerebral palsy (CP) was diagnosed if abnormalities in neuromotor exam and delayed motor function17 were found, and was classified depending on Gross Motor Function Classification Scale scores, mild (<2), moderate (2–3), and severe (≥4). Evaluators were certified yearly for the neurologic assessment. Methods for these measures and for establishing interrater reliability on all assessments have been reported previously.17
The Brief Infant and Toddler Social and Emotional Assessment (BITSEA) was used to identify potential behavioral problems or delays in socioemotional competence.15 The BITSEA is a standardized screening questionnaire consisting of 42 items, derived from the 169-item Infant Toddler Social and Emotional Assessment.18 The BITSEA is a short, easy-to-administer, and reliable screen for socioemotional assessment that has been validated in the United States19–21 and in other countries.22–25 The BITSEA has 2 separate scales: problem and competence. The problem scale includes behaviors that may become problematic (for example, aggression, sadness, or fear). Socioemotional competence items address areas of attention, compliance, mastery motivation, prosocial skills, empathy, imitation/play skills, and social relatedness. Both scales also include atypical behaviors often seen in children with autism spectrum disorder (ASD). The study coordinators assisted primary caregivers in completing the BITSEA by reading the questionnaire verbatim to them during their clinic visit.
Individual BITSEA items are rated on a 3-point scale as not true/rarely (0), somewhat true/sometimes (1), or very true/often (2), yielding a total score and cut points for each scale. Significant behavioral problems were present if the problem score obtained was ≥75th percentile. Competence deficits were present if competence scores were ≤15th percentile. For this study, scores were determined according to CA and sex. Good test-retest reliability has been demonstrated for the BITSEA with intraclass correlations of 0.82 for the problem scale and 0.72 for the competence scale. The BITSEA has been validated against the Child Behavior Checklist and has also been shown to correlate with parents’ reports of parental worry, stress, and interference in family life. The BITSEA is also a good predictor for behavioral problems 1 year later26 and at school age.21
The Bayley-III was administered by yearly certified examiners to assess cognitive and language (composite expressive and receptive) functioning. Bayley-III scores were assessed relative to a standardized mean (±SD) of 100 ± 15, with higher scores indicating better performance.27
Data from the NICHD NRN are collected in each center on standard forms and are compiled at the data coordinating center, RTI International (Research Triangle Park, NC). Institutional review boards at each center approved the study. RTI personnel assessed data completion and consistency. Data analysis was performed by using SAS version 9.1 (SAS Institute, Inc, Cary, NC). Problem and competence scores, socioemotional competence scores, and percentage of children meeting the cutoff points for both indices were computed by sex and were compared with a reference group by using Student’s t tests and χ2 tests. Bivariate relationships between demographic and medical risk factors and problem and competence scores on the BITSEA were examined by using χ2 tests for categorical variables and t tests for continuous variables. Logistic regression analyses were used to assess the impact of infant (ie, GA, BW, multiple birth, BPD [defined as requiring oxygen at 36 weeks’ postmenstrual age], discharge or transfer, whichever came first, IVH grade 3 or 4, periventricular leukomalacia, sex, race, and CP diagnosis or an abnormal neurologic exam at 18 to 22 months’ CA) and maternal/demographic (ie, marital status, education, age, public insurance status at 18 to 22 months visit, and household income) risk factors on the presence of behavioral problems and deficits in socioemotional competence. Structural equation modeling was used to test whether Bayley-III cognitive and language development composite scores mediated the relationship between risk factors and behavioral problems and socioemotional competence scores. These models were fit by using the Mplus software program28 with bootstrapping to calculate the confidence intervals for the mediation effects.29
At 18 to 22 months’ CA, the EP children scored significantly worse on the problem scale compared with norms for both boys and girls. The percentage of children with behavioral problems or deficits in socioemotional competence using the designated cutoff point was higher than expected based on the reference normative group (Table 1).
In the bivariate analysis (Table 2), child factors associated with behavioral problems (P < .05) were multiple birth, male sex, race, and rehospitalization. The maternal characteristics associated with behavioral problems included maternal age, maternal education less than HS, being unmarried, having public health insurance, and living arrangements if living with the biological mother only. Factors independently associated with behavioral problems included male sex, having public medical insurance, lower maternal education, and lower maternal age after controlling for demographic and other factors (Table 3) by using logistic regression models.
Using bivariate analysis, child factors associated with competence deficits included lower BW, race, rehospitalization, and abnormal neurologic examination or the diagnosis of CP at 18 to 22 months. Maternal characteristics associated with competence deficits were lower maternal education and having public health insurance. Child characteristics associated with competence deficits included rehospitalization and/or abnormal neurologic exam or moderate to severe CP at 18 to 22 months’ CA (Table 2).
Using logistic regression models and controlling for other factors, lower BW, having public medical insurance, maternal education less than HS, and having an abnormal neurologic exam at 18 to 22 months were independently associated with competence problems (Table 3).
Relationship Between BITSEA and Bayley-III
Bayley-III cognitive and language scores were lower in children with behavioral problems or deficits in competence (Table 4). Children with behavioral problems had lower mean Bayley-III cognitive and language composite scores than children without behavioral problems. A higher percentage of children with behavioral problems had cognitive scores <85 and composite language scores <85 and <70. More children with competence deficits had Bayley-III cognitive scores <85 or 70 or language scores <85 or 70 than those without deficits (P < .05).
Bayley-III composite language score mediated the relationship between behavioral problems and male sex, public insurance, maternal education less than HS, and lower maternal age; cognitive scores were significant mediators for all of the above except maternal age (Table 5). Both Bayley-III cognitive and composite language scores were mediators of the relationship between competence deficits and low BW, public insurance, maternal education less than HS, and abnormal neurologic exam (Table 6).
This study evaluated behavioral problems and socioemotional competence and associated risk factors in a large sample of EP children at 18 to 22 months’ CA. Our results indicate that children born EP are at increased risk for behavioral problems and deficits in socioemotional competence when compared with population norms and that risk factors that are associated with poor outcomes can be identified at an earlier age.
Research regarding behavioral problems in EP children has been inconsistent and typically has focused on children older than our sample population.30 Our finding of a substantial proportion of EP children with behavioral problems and socioemotional competence deficits is comparable to another previous study that compared very preterm children to a term sample of children 3 years of age in France by using the Strengths and Difficulties Questionnaire.31 We previously reported a high prevalence of behavioral and socioemotional problems in a similar sample of 30-month-old ELBW children.13 Previous reports suggest that 46% to 50% of children who had behavioral problems at 3 years of age continue to have behavior problems at 5 years of age.32,33 Thus, the high rates of behavioral problems and socioemotional deficits already evident by 18 to 22 months are important, because earlier behavioral intervention potentially can be initiated to prevent later problems.
Certain infant characteristics, such as being a boy, and maternal characteristics, such as young maternal age, lower maternal education, being unmarried, and receiving public health insurance assistance, were associated with behavioral problems and deficits in socioemotional competence. Previous studies have found that socioeconomic status, the quality of the home environment, and maternal education are related to behavioral disorders and cognitive development.34 The quality of the home environment may support parent-child interactions and assist a child in developing self-regulated behaviors like maintaining attention or inhibiting impulsive responses. Deficits in socioemotional competence were associated with lower maternal education and receiving public health insurance. Several studies have reported that financial and emotional stressors associated with poverty negatively affect parenting behaviors, leading to subsequent cognitive and behavioral problems in children.35 Male sex was associated with behavioral problems in the current study. Although findings of a higher prevalence of behavior problems in boy preschool-age children has been evident in community samples,36,37 previous studies of premature children have not been consistent regarding increased behavioral problems in boys. Some studies have demonstrated a higher rate of behavioral problems in premature girls. We reported previously a slight increase in behavioral problems at 30 months of age in girls compared with boys in a group of children who were born at ELBW.13 A similar finding was also reported in a study of very low BW children at 2 years of age.38 However, male sex has been associated with overall poorer developmental outcomes in preterm infants.39–41 Another previous study using the Behavior Rating Scale of the Bayley Scales of Infant and Toddler Development, Second Edition reported more socioemotional problems in boys at 2 years of age.42 GA has been associated with adverse neurodevelopmental outcomes. In our study, neither behavioral problems nor competence deficits were associated with GA. However, competence deficits were associated with lower BW. Our sample only included children from 23 to <27 weeks’ gestation; this narrow range of GA may make it difficult to detect differences related to GA. Our previous study of ELBW children did not find an association between BW or GA and behavioral and socioemotional outcomes at 30 months of age.13 Other studies of behavioral problems at an early age also did not find an effect of GA.31 Lower BW was associated with competence deficits in our study. Perhaps this reflects the effects of intrauterine growth restriction on children born at lower BW. Others have reported poorer neurodevelopmental outcomes in preterm children born after intrauterine growth restriction.43,44
An abnormal neurologic exam at 18 months of age was associated with competence deficits. Cerebral lesions as detected by head ultrasound during the neonatal period did not correlate with behavioral or socioemotional difficulties in our study, although early cranial ultrasound may not detect significant brain abnormalities or predict neurodevelopmental outcome when compared with near-term cranial ultrasound or MRI.45,46 Despite advances in neuroimaging of preterm infants, few studies have correlated behavioral disorders with brain abnormalities on imaging. However, children with attention-deficit/hyperactivity disorder who were born preterm have been reported to have abnormal neonatal imaging studies.47 Some studies have reported an association of neuromotor problems with cognitive and behavioral disorders.42,44
We found that Bayley-III cognitive and composite language scores are significant intervening mediating variables in the occurrence of socioemotional deficits. Self-regulation, a component of socioemotional development, is thought to be associated with positive developmental outcomes in children, including better cognitive abilities. In addition, language development may support the development of self-regulation skills in young children.48 With increased knowledge of socioemotional development in preterm children, we can identify appropriate targets for effective early intervention.
Previous studies have reported an increased incidence of ASD in children born ELBW.49 However, interpreting this association is complicated given the increased prevalence of developmental delays in children who were ELBW at birth.50–52 Both behavioral problems and competence deficits have been associated with ASD.15 The BITSEA includes items associated with ASD (eg, social relatedness, social withdrawal, and repetitive behaviors). In particular, competence scores have been suggested as an effective tool for ASD screening.53 The NICHD NRN follow-up cohort study has not evaluated comprehensively for ASD in this group of EP children. The question of whether a possible diagnosis of ASD had been communicated to the parents by a medical professional was added to the data collection form in the last 2 years of the study period.
The BITSEA is a screening checklist that is completed only by the primary caregiver or parent. Thus, it reflects only the perception of the primary caregiver,54 who may be influenced by other factors, such as their own mental health. Indeed, many studies have reported that mothers with mental health problems report more problems in their children than mothers without mental health problems.55,56 To obtain a comprehensive assessment of children’s behavioral and socioemotional functioning, multimodal assessment is recommended using structured diagnostic interviews and checklists from several raters.57 Some caregivers may have had difficulty understanding the BITSEA items, particularly those that are reverse-keyed. However, to minimize misunderstanding, especially for caregivers with low reading ability, the survey was administered by trained research staff. Second, we did not have a term control group; however, we compared our scores to published norms from the standardization sample of the BITSEA. We acknowledge that the sample used for this standardization sample was likely different than our sample. However, this was a large cohort of EP children drawn from different centers around the United States. Assessments were not completed blinded to perinatal history and varied by center. However, BITSEA results were not usually known by examiners because scores were calculated later. Finally, although the BITSEA is only a screener, it correlates well with the ITSEA, the longer version of the scale, has been tested in different populations, and has been shown to be valid and effective in the detection of behavioral problems and socioemotional deficits in preschool-aged children.
EP children are at risk not only for general developmental problems, but also for behavioral problems and deficits in socioemotional competence by 18 to 22 months’ CA. Early identification of these problems before 2 years of age would enable intervention within the second year of life. If these difficulties persist into school age, they are likely to hinder children’s cognitive functioning as well as school performance and overall functional outcomes. Additional research to determine if these behavior problems persist long-term is recommended. Environmental variables, including caregiver education, family functioning, and family social support, have a significant impact on behavioral and socioemotional outcomes of these children. Because behavioral and socioemotional development can impact the developmental trajectories of children who are born at high risk, socioemotional development should be assessed when these children are clinically evaluated to elucidate targeted interventions to be implemented in this vulnerable population.
Although National Institute of Child Health and Human Development staff did have input into the study design, conduct, analysis, and manuscript drafting, the content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Data collected at participating sites of the National Institute of Child Health and Human Development Neonatal Research Network were transmitted to RTI International, the data coordinating center (DCC) for the network, which stored, managed, and analyzed the data for this study. On behalf of the Neonatal Research Network, Drs Abhik Das (DCC principal investigator) and Carla Bann (DCC statistician) had full access to all the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis.
We thank our medical and nursing colleagues and the infants and their parents who agreed to take part in this study. The following investigators, in addition to those listed as authors, participated in this study:
NRN Steering Committee Chairs: Michael S. Caplan, MD, University of Chicago, Pritzker School of Medicine (2006–2011); Richard A. Polin, MD, Division of Neonatology, College of Physicians and Surgeons, Columbia University (2011 to present).
Alpert Medical School of Brown University and Women & Infants Hospital of Rhode Island (U10 HD27904): Abbot R. Laptook, MD; Martin Keszler, MD; William Oh, MD; Betty R. Vohr, MD; Angelita M. Hensman, MS, RNC-NIC; Kristin M. Basso, BSN MaT; Barbara Alksninis, PNP; Robert Burke, MD; Melinda Caskey, MD; Andrea Halbrook; Katharine Johnson, MD; Mary Lenore Keszler, MD; Theresa M. Leach, Med, CAES; Bonnie E. Stephens, MD; Suzy Ventura; and Victoria E. Watson, MS, CAS.
Case Western Reserve University, Rainbow Babies & Children’s Hospital (U10 HD21364, M01 RR80): Michele C. Walsh, MD, MS; Avroy A. Fanaroff, MD; Anna Marie Hibbs, MD; Deanne E. Wilson-Costello, MD; Nancy S. Newman, BA, RN; Bonnie S. Siner, RN; Monika Bhola, MD; Gulgun Yalcinkaya, MD; and Harriet G. Friedman, MA.
Children’s Mercy Hospital (U10 HD68284): William E. Truog, MD; Eugenia K. Pallotto, MD, MSCE; Howard W. Kilbride, MD; Cheri Gauldin, RN, MSN, CCRC; Anne Holmes, RN, MSN, MBA-HCM, CCRC; and Kathy Johnson, RN, CCRC.
Cincinnati Children’s Hospital Medical Center, University Hospital, and Good Samaritan Hospital (U10 HD27853, M01 RR8084): Kurt Schibler, MD; Edward F. Donovan, MD; Cathy Grisby, BSN, CCRC; Barbara Alexander, RN; Kate Bridges, MD; Estelle E. Fischer, MHSA, MBA; Teresa L. Gratton, PA; Holly L. Mincey, RN, BSN; Greg Muthig, BS; Jody Hessling, RN; Teresa L. Gratton, PA; Lenora D. Jackson, CRC; Kristin Kirker, CRC; and Kimberly Yolton, PhD.
Duke University School of Medicine, University Hospital, University of North Carolina, and Duke Regional Hospital (U10 HD40492, M01 RR30, UL1 TR83): Ronald N. Goldberg, MD; C. Michael Cotten, MD, MHS; Ricki F. Goldstein, MD; Joanne Finkle, RN, JD; Patricia L. Ashley, MD, PhD; William F. Malcolm, MD; Kathy J. Auten, MSHS; Kimberley A. Fisher, PhD, FNP-BC, IBCLC; Katherine A. Foy, RN; Sandra Grimes, RN, BSN; Melody B. Lohmeyer, RN, MSN; Matthew M. Laughon, MD, MPH; Carl L. Bose, MD; Janice Bernhardt, MS, RN; Gennie Bose, RN; and Janice K. Wereszczak, CPNP-AC/PC.
Emory University, Children’s Healthcare of Atlanta, Grady Memorial Hospital, and Emory University Hospital Midtown (U10 HD27851, M01 RR39, UL1 TR454): Barbara J. Stoll, MD; David P. Carlton, MD; Ira Adams-Chapman, MD; Ellen C. Hale, RN, BS, CCRC; Yvonne C. Loggins, RN, BSN; Maureen Mulligan LaRossa, RN; and Sheena L. Carter, PhD.
NICHD: Rosemary D. Higgins, MD; and Stephanie Wilson Archer, MA.
Indiana University, University Hospital, Methodist Hospital, Riley Hospital for Children, and Wishard Health Services (U10 HD27856, M01 RR750, UL1 TR6): Gregory M. Sokol, MD; Brenda B. Poindexter, MD, MS; Anna M. Dusick, MD (deceased); Lu-Ann Papile, MD; Dianne E. Herron, RN; Lucy C. Miller, RN, BSN, CCRC; Carolyn Lytle, MD, MPH; Ann B. Cook, MS; Heike M. Minnich, PsyD, HSPP; Abbey C. Hines, PsyD; Leslie Dawn Wilson, BSN, CCRC; and Faithe Hamer, BS.
Nationwide Children’s Hospital and the Ohio State University Medical Center (U10 HD68278): Pablo J. Sánchez, MD; Leif D. Nelin, MD; Sudarshan R. Jadcherla, MD; Patricia Luzader, RN; Christine A. Fortney, PhD, RN; Gail E. Besner; and Nehal A. Parikh, MD.
RTI International (U10 HD36790): Abhik Das, PhD; Dennis Wallace, PhD; W. Kenneth Poole, PhD (deceased); Jeanette O’Donnell Auman, BS; Margaret M. Crawford, BS, CCRP; Marie G. Gantz, PhD; Carolyn M. Petrie Huitema, MS, CCRP; and Kristin M. Zaterka-Baxter, RN, BSN, CCRP.
Stanford University, Dominican Hospital, El Camino Hospital, and Lucile Packard Children’s Hospital (U10 HD27880, M01 RR70, UL1 TR93): Krisa P. Van Meurs, MD; David K. Stevenson, MD; Susan R. Hintz, MD, MS, Epi; M. Bethany Ball, BS, CCRC; Marian M. Adams, MD; Barbara Bentley, PhD; Elizabeth Bruno, PhD; Maria Elena DeAnda, PhD; Anne M. DeBattista, RN, PNP; Lynne C. Huffman, MD; Jean G. Kohn, MD, MPH; Casey E. Krueger, PhD; Andrew W. Palmquist, RN; Melinda S. Proud, RCP; Brian Tang, MD; and Hali E. Weiss, MD.
Tufts Medical Center, Floating Hospital for Children (U10 HD53119, M01 RR54): Ivan D. Frantz III, MD; John M. Fiascone, MD; Elisabeth C. McGowan, MD; Brenda L. MacKinnon, RNC; Ana K. Brussa, MS, OTR/L; Anne Furey, MPH; Ellen Nylen, RN, BSN; and Cecelia E. Sibley, PT, MHA.
University of Alabama at Birmingham Health System and Children’s Hospital of Alabama (U10 HD34216, M01 RR32): Namasivayam Ambalavanan, MD; Monica V. Collins, RN, BSN, MaEd; Shirley S. Cosby, RN, BSN; Fred J. Biasini, PhD; Kristy Domnanovich, PhD; Kristen C. Johnston, MSN, CRNP; Carin Kiser, MD; Sara Kryzwanski, MS; Kathleen G. Nelson, MD; Cryshelle S. Patterson, PhD; Richard V. Rector, PhD; Leslie Rodrigues, PhD; Sarah Ryan, PhD; Leigh Ann Smith, CRNP; Amanda D. Soong, MD; and Sally Whitley, MA, OTR-L, FAOTA.
University of California, Los Angeles, Mattel Children’s Hospital, Santa Monica Hospital, Los Robles Hospital and Medical Center, and Olive View Medical Center (U10 HD68270): Uday Devaskar, MD; Meena Garg, MD; Isabell B. Purdy, PhD, CPNP; Teresa Chanlaw, MPH; and Rachel Geller, RN, BSN.
University of California, San Diego Medical Center and Sharp Mary Birch Hospital for Women and Newborns (U10 HD40461): Neil N. Finer, MD; David Kaegi, MD; Maynard R. Rasmussen, MD; Kathy Arnell, RNC; Clarence Demetrio, RN; Martha G. Fuller, RN, MSN; Chris Henderson, RCP, CRTT; Wade Rich, BSHS, RRT; and Radmila West, PhD.
University of Iowa and Mercy Medical Center (U10 HD53109, M01 RR59): Edward F. Bell, MD; Dan L. Ellsbury, MD; John A. Widness, MD; Tarah T. Colaizy, MD, MPH; Michael J. Acarregui, MD; Jane E. Brumbaugh, MD; Karen J. Johnson, RN, BSN; Donia B. Campbell, RNC-NC; Diane L. Eastman, RN, CPNP, MA; and Jacky R. Walker, RN.
University of Miami, Holtz Children’s Hospital (U10 HD21397, M01 RR16587): Shahnaz Duara, MD; Charles R. Bauer, MD; Ruth Everett-Thomas, RN, MSN; Sylvia Fajardo-Hiriart, MD; Arielle Rigaud, MD; Maria Calejo, MS; Silvia M. Frade Eguaras, MA; Michelle Harwood Berkowits, PhD; Andrea Garcia, MS; Helina Pierre, BA; and Alexandra Stoerger, BA.
University of New Mexico Health Sciences Center (U10 HD53089, M01 RR997, UL1 TR41): Kristi L. Watterberg, MD; Robin K. Ohls, MD; Janell F. Fuller, MD; Conra Backstrom Lacy, RN; Sandra Brown, BSN; Carol Hartenberger, BSN, MPH; Jean R. Lowe, PhD; and Rebecca A. Montman, BSN, RNC.
University of Pennsylvania, Hospital of the University of Pennsylvania, Pennsylvania Hospital, and Children’s Hospital of Philadelphia (U10 HD68244): Barbara Schmidt, MD, MSc; Haresh Kirpalani, MB, MSc; Sara B. DeMauro, MD, MSCE; Aasma S. Chaudhary, BS, RRT; Soraya Abbasi, MD; Toni Mancini, RN, BSN, CCRC; Dara M. Cucinotta, RN; Judy C. Bernbaum, MD; Marsha Gerdes, PhD; and Hallam Hurt, MD.
University of Rochester Medical Center, Golisano Children’s Hospital, the University of Buffalo Women’s, and Children’s Hospital of Buffalo (U10 HD68263, U10 HD40521, UL1 RR24160, M01 RR44, UL1 TR42): Carl T. D’Angio, MD; Dale L. Phelps, MD; Ronnie Guillet, MD, PhD; Gary J. Myers, MD; Linda J. Reubens, RN, CCRC; Erica Burnell, RN; Diane Hust, MS, RN, CS; Julie Babish Johnson, MSW; Julianne Hunn, BS; Rosemary L. Jensen; Emily Kushner, MA; Deanna Maffett, RN; Joan Merzbach, LMSW; Holly I.M. Wadkins; Kelley Yost, PhD; Lauren Zwetsch, RN, MS, PNP; Satyan Lakshminrusimha, MD; Anne Marie Reynolds, MD, MPH; Farooq Osman, MD; Ashley Williams, MSEd; and Karen Wynn, RN.
University of Texas Health Science Center at Houston Medical School, Children’s Memorial Hermann Hospital, and Lyndon Baines Johnson General Hospital/Harris County Hospital District (U10 HD21373): Kathleen A. Kennedy, MD, MPH; Jon E. Tyson, MD, MPH; Georgia E. McDavid, RN; Nora I. Alaniz, BS; Katrina Burson, RN, BSN; Patricia W. Evans, MD; Charles Green, PhD; Beverly Foley Harris, RN, BSN; Margarita Jiminez, MD, MPH; Anna E. Lis, RN, BSN; Sarah Martin, RN, BSN; Brenda H. Morris, MD; M. Layne Poundstone, RN, BSN; Peggy Robichaux, RN, BSN; Saba Siddiki, MD; Maegan C. Simmons, RN; Patti L. Pierce Tate, RCP; and Sharon L. Wright, MT(ASCP).
University of Texas Southwestern Medical Center at Dallas, Parkland Health & Hospital System, and Children’s Medical Center Dallas (U10 HD40689, M01 RR633): Pablo J. Sánchez, MD; Luc P. Brion, MD; Roy J. Heyne, MD; Walid A. Salhab, MD; Charles R. Rosenfeld, MD; Diana M. Vasil, RNC-NIC; Sally S. Adams, MS, RN, CPNP; Lijun Chen, PhD, RN; Alicia Guzman; Gaynelle Hensley, RN; Elizabeth T. Heyne, MS, MA, PA-C, PsyD; Melissa H. Leps, RN; Linda A. Madden, RN, CPNP; Nancy A. Miller, RN; Janet S. Morgan, RN; Lizette E. Torres, RN; and Catherine Twell Boatman, MS, CIMI.
University of Utah Medical Center, Intermountain Medical Center, LDS Hospital, and Primary Children’s Medical Center (U10 HD53124, M01 RR64, UL1 TR105): Roger G. Faix, MD; Bradley A. Yoder, MD; Anna Bodnar, MD; Karen A. Osborne, RN, BSN, CCRC; Shawna Baker, RN; Karie Bird, RN, BSN; Jill Burnett, RNC, BSN; Laura Cole, RN; Jennifer J. Jensen, RN, BSN; Cynthia Spencer, RNC; Michael Steffen, MS, CPM; Kimberlee Weaver-Lewis, RN, BSN; Sarah Winter, MD; and Karen Zanetti, RN.
Wake Forest University, Baptist Medical Center, Forsyth Medical Center, and Brenner Children’s Hospital (U10 HD40498, M01 RR7122): T. Michael O’Shea, MD, MPH; Robert G. Dillard, MD; Lisa K. Washburn, MD; Barbara G. Jackson, RN, BSN; Nancy Peters, RN; Korinne Chiu, MA; Deborah Evans Allred, MA, LPA; Donald J. Goldstein, PhD; Raquel Halfond, MA; Carroll Peterson, MA; Ellen L. Waldrep, MS; Cherrie D. Welch, MD, MPH; Melissa Whalen Morris, MA; and Gail Wiley Hounshell, PhD.
Wayne State University, Hutzel Women’s Hospital, and Children’s Hospital of Michigan (U10 HD21385): Seetha Shankaran, MD; John Barks, MD; Rebecca Bara, RN, BSN; Angela Argento; PhD; Martha Carlson, MD; Laura A. Goldston, MA; Mary Johnson, RN, BSN; Mary Christensen, RT; and Stephanie Wiggins, MS.
Yale University, Yale-New Haven Children’s Hospital, and Bridgeport Hospital (U10 HD27871, UL1 RR24139, M01 RR125, UL1 TR142): Richard A. Ehrenkranz, MD; Harris Jacobs, MD; Christine G. Butler, MD; Patricia Cervone, RN; Sheila Greisman, RN; Monica Konstantino, RN, BSN; JoAnn Poulsen, RN; Janet Taft, RN, BSN; Joanne Williams, RN, BSN; and Elaine Romano, MSN.
- Accepted February 28, 2017.
- Address correspondence to Myriam Peralta-Carcelen, MD, MPH, Division of Developmental and Behavioral Pediatrics, University of Alabama at Birmingham, 5602 Dearth Tower, 1600 7th Ave S, Birmingham, AL 35233. E-mail:
This trial has been registered at www.clinicaltrials.gov (identifier NCT00063).
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: The National Institutes of Health, the Eunice Kennedy Shriver National Institute of Child Health and Human Development, the National Center for Research Resources, and the National Center for Advancing Translational Sciences provided grant support for the Neonatal Research Network’s Generic Database and Follow-up Studies through cooperative agreements. Cooperative agreements are listed by institution in the acknowledgements section. Funded by the National Institutes of Health (NIH).
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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- Copyright © 2017 by the American Academy of Pediatrics