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Early Human Development 89 (2013) 925–930
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Early Human Development
j ourna l homepage: www.e lsev ie r .com/ locate /ear lhumdev
Social–emotional delays at 2 years in extremely low gestational agesurvivors: Correlates of impaired orientation/engagement and emotional regulation
Lauren A.C. Boyd a, Michael E. Msall b,⁎, T. Michael O'Shea c, Elizabeth N. Allred d,e,f,Gail Hounshell c, Alan Leviton d,e
a Department of Pediatrics, Loyola University Medical Center and Loyola University of Chicago Stritch School of Medicine, Maywood, IL, United Statesb Kennedy Research Center on Intellectual andDevelopmental Disabilities, Section of Developmental and Behavioral Pediatrics, University of Chicago Comer Children's Hospitals, Chicago, IL, United Statesc Department of Pediatrics, Wake Forest School of Medicine, Winston-Salem, NC, United Statesd Department of Neurology, Harvard Medical School, Boston, MA, United Statese Department of Neurology, Boston Children's Hospital, Boston, MA, United Statesf Department of Biostatistics, Harvard School of Public Health, Boston, MA, United States
Abbreviations: ELGAN, Extremely Low GestationalRegulation; O/E, Orientation Engagement; NO/Q, non-opBayley Scales Infant Development-II; BRS, BehaviorDevelopment Index; PDI, Psychomotor DevelopmentFunction Classification System; IVH, intraventricular hem⁎ Corresponding author at: 950 E 61st St., SSC 207, Ch
Tel.: +1 773 702 3095; fax: +1 773 702 0208.E-mail address: [email protected] (M.E.
0378-3782/$ – see front matter © 2013 Published by Elsehttp://dx.doi.org/10.1016/j.earlhumdev.2013.09.019
a b s t r a c t
a r t i c l e i n f oArticle history:
Received 22 August 2013Accepted 23 September 2013Keywords:Extreme prematurityBehavioral regulationBrain injuryNeurodevelopmental disability
Background: Premature infants are less socially and emotionally competent at school age than infants born atterm.Aims: To evaluate the correlates of social and emotional delays at 2 years of age among prematurely born children.Study design: This is a prospective cohort study.Subjects: 904 children born at b28 weeks gestation during 2002–2004 and enrolled in the ELGAN study who sur-vived until age 2 years and returned for a developmental assessment.Outcome measures: The Bayley Behavior Rating Scale (BRS), a neurological examination, and the Bayley Scales ofInfant Development II (BSID-II).
Results: Fully 31% of children had a non-optimal (14%) or questionable (17%) (NO/Q) BRS score for Emotional Reg-ulation (ER), and 27% had a non-optimal (13%) or questionable (14%) score for Orientation/Engagement (O/E). Chil-drenwithNO/Q scores on ER andO/Eweremore likely than others to haveMDI and PDI scoresb70 and beunable towalk. Antecedents of NO/Q OE scores includedmulti-fetal pregnancy, while antecedents of NO/Q scores for both ERand O/E included indicators of socioeconomic disadvantage, and male sex.Conclusions: Over 25% of children born extremely premature exhibit socio-emotional delays during developmentalassessment at age 2 years. Antecedents of these delays include sociodemographic characteristics, as well as thosecommon antecedents of other impairments commonly observed among extremely preterm infants.© 2013 Published by Elsevier Ireland Ltd.
1. Introduction
Traditional follow up of premature infants has focused on grossmotorand cognitive development. As cohorts of premature infants have ma-tured, additional vulnerability to behavioral and mental health disordershas been identified. Compared to children born at term, preterm infantsare at increased risk of attention deficit hyperactivity disorder (ADHD),anxiety, depression, and behavior problems in middle childhood andadolescence [1–10]. Social–emotional development, which includes theability to engage, explore, handle frustration, self regulate and develop
Age Newborn; ER, Emotionaltimal or questionable; BSID-II,Rating Scale; MDI, MentalIndex; GMFCS, Gross Motor
orrhage.icago, IL 60637, United States.
Msall).
vier Ireland Ltd.
relationships with peers and adults, is now beginning to receive more at-tention. However, reliable and valid evaluations of behavioral competen-cies have not been applied to large prospective cohorts [1].
The Bayley Scales of Infant Development, second edition (BSID-II)includes the Behavior Rating Scale (BRS), an observer rating scale thatassesses both orientation/engagement (exploration, initiative, engage-ment with testing) and emotional regulation (persistence, frustration,cooperation, attention to testing) based on observing children's playwith a variety of toys, puzzles, and pictures during the Bayley assessment.BRS scores are reported as within normal limits (26–99 percentiles),questionable (11–25th percentile) and non-optimal (less than the 11thpercentile).
To our knowledge, only one study has described antecedents andcorrelates of percentile scores of the total BRS in very low birth weightchildren [11]. In this study, we sought to identify the antecedents andcorrelates of non-optimal or questionable BRS scores for Emotional Reg-ulation (ER), and of non-optimal (NO) or questionable (Q) scores forOrientation/Engagement (O/E) in a sample of 904 children at age2 years who were born before the 28th week of gestation.
926 L.A.C. Boyd et al. / Early Human Development 89 (2013) 925–930
2. Methods
2.1. The ELGAN study
The ELGAN study was designed to identify factors that increase therisk for neurodevelopmental disorders in Extremely Low GestationalAge Newborns (ELGANs). From 2002–2004, 1506 babies born atb28 weeks gestation to 1249 mothers were enrolled at one of the 14participating institutions in 5 states. The enrollment and consent pro-cesses were approved by the individual institutional review boards.The 904 children who had a BRS assessment at age 2 years are the sub-jects of this report (see Fig. 1).
Demographic and pregnancy characteristics were obtained frommaternal interview and chart review. The clinical circumstances thatled to preterm delivery were defined [12] and each mother/infant pairwas assigned to the category that described the primary reason for pre-term delivery. Review of the newborn's chart provided details about herclinical course in the intensive care nursery.
The gestational age (GA) estimates were based on a hierarchy ofavailable information. Estimates were considered most desirable iftheywere based on the dates of embryo retrieval or intrauterine insem-ination or fetal ultrasound before the 14th week and less desirable ifbased on a later fetal ultrasound and LMP without fetal ultrasound.
The birth weight (BW) Z-score is the number of standard deviationsthe infant's BW is above or below the median weight of infants at thesame GA in referent samples not delivered for preeclampsia or fetal in-dications [13,14].
Ultrasound scans of the brain were obtained according to protocoland read concordantly by two sonologists. Details about observer vari-ability minimization efforts and the definitions of lesions are presentedelsewhere [15].
2.2. The 24-month developmental assessment
Fully 91% of surviving children returned for the developmental assess-ment. Of these children, 77% had their exam within the range of 23.5–27.9 months postmenstrual age, 14% were assessed before 23.5 months,and 12% were assessed after 27.9 months. At that time, children receiveda full neurological exam and were assigned a Gross Motor Function Clas-sification System (GMFCS) level [16]. They were also assessed with theBayley Scales of Infant Development, second edition (BSID-II), includingthe Behavior Rating Scale (BRS). The child's caregiver was asked to com-plete a detailed interval medical history questionnaire. Caregivers whodid not speak English were provided with a translator for interviewsand questionnaire completion.
Fig. 1. Extremely Low Gestation Age Newborns (ELGANs): 2 ye
2.3. BSID-II
Certified examiners administered the Mental Development Index(MDI) and Psychomotor Development Index (PDI) of the BSID-II. To de-crease inter-examiner variability, all BSID-II examiners attended a one-day workshop in which test administration was discussed. Videoclipswere used to demonstrate the correct administration of specific testitems. After approximately one-half of the study participants had beenexamined, BSID examiners completed a written test of their knowledgeabout how to administer specific test items and received feedback ontheir responses. The examiners were aware of the infants' enrollmentin the ELGAN study but were not informed of their medical history. Be-fore testing, the examiner was given the child's corrected age. Wetrichotomized both MDI and PDI at b55 (more than three standard de-viations below the expected mean), 55–69 (more than two, but lessthan three standard deviations below the expected mean), and ≥70.The child was classified as non-testable if her impairments precludedstandardized administration. If the examiners judged more than 2 itemsas not applicable the child was excluded from the current study. On thebasis of their composite score on the Vineland Adaptive Behavior Scales(VABS), 12 children considered non-testable were assigned an MDIequivalent of b70 (N = 3) or ≥70 (N = 9). On the basis of the MotorSkills domain scale score of the VABS, 18 considered non-testable wereassigned a PDI equivalent of b70 (N = 9) or ≥70 (N = 9).
After administering the BSID-II, the examiner rated the child usingtwo factors of the BRS, the Orientation/Engagement factor (exploration,initiative, engagement with testing), and the Emotional Regulation fac-tor (persistence, frustration, cooperation, attention to testing) [17]. TheBRS scale also includes an assessment of motor quality and a total score.Because we had a completed neurological examination as part of thestudy, the motor quality score was not included in our data analysis. Atotal BRS score can be calculated, but it is affected by the motor qualityscore; therefore, we chose to focus on the orientation/engagement andemotional regulation factor scores only. The examiner rated the child'sbehavior on a 5-point scale. The total raw scores were categorized:within normal limits (26–99 percentiles), questionable (Q) (11–25thpercentile) and non-optimal (NO) (less than 11th percentile).
2.4. Neurological examination
The neurological examination was completed by a trained clini-cian using an explicit approach with documented low inter-examinervariability [18]. An algorithm assigned each child with a significantmotor limitation to themost appropriate topographic phenotype of quad-riparetic, diparetic, or hemiparetic cerebral palsy [19]. Only 4% of
ar behavioral, neurological and developmental outcomes.
Table 1Maternal and social characteristics and BRS score.
Maternal characteristics Orientation/Engagement
EmotionalRegulation
Row
NO QU p NO QU p N
Racial identity White 12 11 .02 13 15 .001 516Black 16 16 19 23 267Other 19 17 12 14 106
Years of education b12 19 14 .12 20 18 .05 14112 (high school) 18 12 17 16 237N12, b16 11 12 13 19 20716 (college) 10 13 8 21 163N16 13 16 14 11 125
Self supported Yes 12 13 .03 12 18 .007 567No 18 13 18 16 298
Public insurance Yes 16 13 .37 19 16 .006 354No 13 13 11 18 532
Maximum number 126 117 129 154 904
The percent of childrenwhosemother had the characteristic listed on the left who had thebehavior rating at the head of each column. These are row percents. Non-optimal = NO,questionable = QU.
Table 2Infant characteristics and BRS score.
Characteristics of the infant Orientation/Engagement
EmotionalRegulation
Row
NO QU p NO QU p N
Sex Male 14 14 .34 16 20 .008 471Female 14 11 12 14 433
Multiple gestation Yes 17 15 .03 13 14 .21 298No 12 12 15 18 606
Gestational age (week) 23–24 13 13 .75 16 18 .91 16625–26 15 12 15 17 43127 13 14 13 17 307
Birth weight (g) ≤750 14 13 .75 13 22 .09 311751–1000 14 14 15 14 417N1000 13 10 14 15 176
Birth weight Z-scorea b−2 18 20 .41 14 29 .11 51−2, b−1 11 14 11 19 115≥−1 14 12 15 16 738
Head circumference Z-scorea b−2 19 12 .77 12 24 .36 75≥−2, b−1 15 14 14 19 197≥−1 13 13 14 15 602
Maximum number 126 117 129 154 904
The percent of children who had the characteristic listed on the left who had thebehavior rating at the head of each column. These are row percents. Non-optimal = NO,questionable = QU.
a Yudkin standard.
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examiners indicated that at the time of the examination they had knowl-edge of brain-imaging studies.
2.5. Gross Motor Function Classification System (GMFCS)
The examiners rated the child's motor function using the GMFCS, sep-arate from the neurological examination. A level of b1 indicates that thechild canwalk independently. A level of≥2 indicates that the child cannotwalk even when her hand is held [16].
2.6. Head circumference
The head circumference was measured as the largest possibleoccipital–frontal circumference at birth and at 24-months corrected age.All head circumferences are presented as Z-scores based on gestationalage at birth and at the approximations of 24 months corrected age.The standard used for the head circumference Z-scores at birth (Yudkin)[13] differed from the standard used to plot head circumference Z-scoresat 24 months (CDC) [20].
2.7. Data analysis
We evaluated the generalized null hypothesis that non-optimal ori-entation/engagement and emotional regulation are not associated withantenatal antecedents, specifically maternal demographic characteris-tics, pregnancy exposures, and characteristics of the newborn.
We also explored the relationship between non-optimal scores onthe two BRS subscales and indicators of neurodevelopmental dysfunctionat age 2 years. These indicators included: cerebral palsy diagnoses,GMFCS ≥ 2, MDI b 55 or 55–69, PDI b 55 or 55–69, and head circumfer-ence Z-score b −2, or in the range between −2 and less than−1.
We calculated Pearson's chi-square or Fisher's exact test to obtain pvalues for the observed row by column distributions.
3. Results
Compared to the 296 survivors who did not have a BRS, the 904 chil-dren with a completed BRS did not differ in gender, plurality, gestationalage, birth weight, birth weight Z-score, SNAP-II, or the frequency of ultra-sound lesions. Fully 31% of children had a non-optimal (14%) or question-able (17%) BRS score for Emotional Regulation and27%had anon-optimal(13%) or questionable (14%) score for Orientation/Engagement.
3.1. Maternal and pre-natal characteristics (Table 1)
Children born to womenwho did not have formal education beyondhigh school, who identified themselves as Black, and who could notsupport themselves financially or receive support from a partner weremore likely to be scored as non-optimal or questionable on EmotionalRegulation. Children born to women who qualified for state-providedhealth insurance were at increased risk of a non-optimal classificationin Emotional Regulation.
3.2. Characteristics of the infant (Table 2)
Boys were at greater risk than girls of non-optimal or questionableemotional regulation. Children born with a sibling were at greater riskof non-optimal or questionable orientation/engagement scores thansingletons. Children who had low scores on either of the BRS domainswere no more likely than others to have been born at low GA, or tohave had a lowBW, lowBWZ-score, or lowhead circumference Z-score.
3.3. Neurodevelopmental correlates (Table 3)
Children who had ventriculomegaly on a brain ultrasound scanwhile in the intensive care nursery were more likely than others to
have a non-optimal or questionable score in orientation/engagementand a non-optimal emotional regulation score. By and large, childrenwho had quadriparetic or hemiparetic cerebral palsy, low MDI, lowPDI, or microcephaly were more likely than others to have a non-optimal or questionable score in orientation/engagement and/or emo-tional regulation. More than half of children with an MDI of less than55 (more than 3 standard deviations below the mean) scored non-optimal or questionable on both the orientation/engagement and emo-tional regulation scales, while the percent was not so extreme for thosewith an MDI of 55–69 (more than 2 standard deviations below themean), but clearly higher than in those with a higher MDI. A similar“dose–response” pattern was seen for PDIs and for 24-month head cir-cumference Z-scores.
3.4. MDI and PDI correlates (Table 4)
By in large, the lower the MDI or PDI, the higher the frequency ofnon-optimal and questionable scores. Indeed, evenwithin one standarddeviation below the mean or higher for MDI and PDI (i.e., ≥85), more
Table 3Neurodevelopmental structural and functional correlations of BRS score.
Neurodevelopmental correlate/diagnosis Orientation/Engagement Emotional Regulation Row
NO QU p NO QU p N
IVHa Yes 16 14 .46 19 18 .08 184No 13 13 13 17 719
Ventriculomegalya Yes 19 19 .08 22 17 .08 86No 13 12 13 17 817
Hyperechoic lesiona Yes 18 13 .28 22 14 .04 119No 13 13 13 17 784
Hypoechoic lesiona Yes 16 16 .61 16 21 .58 62No 14 13 14 17 881
Cerebral palsy diagnosisb Quadriparesis 31 12 .04 24 19 .37 42Diparesis 16 6 13 16 31Hemiparesis 17 17 8 33 12No CP 13 13 14 16 807
GMFCS ≥2 42 18 ≤ .001 27 30 .003 33b2 13 12 14 16 857
MDI b55 31 26 ≤ .001 31 31 ≤ .001 14455–69 18 14 22 20 94≥70 10 10 8 14 658
PDI b55 29 16 ≤ .001 29 25 ≤ .001 14055–69 22 17 18 25 138≥70 9 11 9 14 610
24 month headcircumferenceZ-scorec
b−2 23 13 .04 21 28 .001 87≥−2, b−1 12 16 12 21 164≥−1 13 11 14 14 626
Maximum number 126 117 129 154 904
The percent of children with a neurodevelopment dysfunction or correlate who had an abnormal BRS rating. These are row percents. Non-optimal = NO, questionable = QU.a On head ultrasound in the NICU.b Among children with GMFCS N 0 and no vision or hearing disability.c CDC standard.
928 L.A.C. Boyd et al. / Early Human Development 89 (2013) 925–930
than 15% of children had a non-optimal or questionable orientation/en-gagement or emotional regulation score.
4. Discussion
We found that over a quarter of extremely preterm infants have im-pairments in engagement and emotional regulation, and that these limi-tations are overrepresented among children with cognitive and motorlimitations, emphasizing the importance of assessing social–emotionalskills, along with motor, sensory, and cognitive functions in earlychildhood. In addition, non-optimal and questionable scores on both theOrientation/Engagement and Emotional Regulation scores were mostcommon among children born to mothers with low socioeconomiccharacteristics, and among boys, while a multi-fetal pregnancy wasalso associated with non-optimal and questionable scores on theOrientation/Engagement scales.
Table 4Relationship between proxy of cognitive and motor development and BRS scores. Theseare row percents.
BSID-II scores Orientation/Engagement Emotional Regulation Row
NO QU p NO QU N
MDI b70 26 21 ≤ .001 28 26 ≤ .001 23870–84 15 12 13 21 225≥85 7 9 6 10 425
PDI b70 26 17 ≤ .001 23 25 ≤ .001 27870–84 14 15 16 13 180≥85 7 10 6 13 430
Maximumnumber
124 115 120 154 888
4.1. BRS construct
The BRS provides a qualitative and quantitative observational impres-sion of the child's behavior during testing thatmaybeused as an indicatorof the child's overall regulatory behavior. Our most prominent findingsare that children with prominent motor and cognitive limitations are athighest risk of sub-optimal scores in orientation/engagement and regula-tory skills [21,22].
Perhaps children with motor impairment appear to be less engagedin the Bayley because of impaired gross and fine motor control. Also,children who have challenges in emotional regulation might scorelower in the mental and psychomotor development indices because oftheir difficulty following an adult-directed lead, or their reluctance to at-tempt test items that appear difficult. In addition, parenting style of achild with multiple disabilities (vulnerable child syndrome) may setup a pattern where the child is not allowed to explore the environmentor take risks, and this may impact her social–emotional development.
4.2. Antecedents
We identified antecedents of non-optimal emotional regulationseparately from those of non-optimal orientation/engagement. However,common risks for challenges in both assessment categories wereidentified. For example, infants born to women experiencing socialdisadvantage (e.g., non-White racial identification, low educationachievement, not able to support themselves or obtain supportfrom family or friends, eligible for state-provided medical insurance)were at increased risk of a non-optimal or questionable score on bothscales. These women often experience greater stressors that disturbparenting routine thereby negatively influencing infant learning of reg-ulatory behaviors [23–25]. The increased demands on mothers caringfor more than one infant might explain our finding that multi-fetal ges-tations were at increased risk of non-optimal or questionable orienta-tion/engagement.
929L.A.C. Boyd et al. / Early Human Development 89 (2013) 925–930
Male sexwas also common to the risk profiles of non-optimal scoreson both scales. We are not sure why this should be, but our findings areconsistent with the higher rate of many developmental delays in pre-maturely bornmales [26–30]. In the one report we could find of the an-tecedents and early correlates of incremental changes of a combinedBRS, boys did not differ appreciably from girls [11].
Gestational age is often a strong predictor of other adverseneurodevelopmental outcomes and is a surrogate for specificdevelopmentally-regulated processes that influence the risk of braininjury [31]. Nevertheless, gestational age was not associated withnon-optimal or questionable scores on the BRS factors of orientation/engagement and emotional regulation. This is surprising, but might re-flect little more than the narrow gestational age range of our subjects.
4.3. Comparison to previous studies
Our study appears to be the first to measure BRS factor scores in alarge, very low gestational age sample without exclusions. Our rates ofabnormal BRS factor scores at age 2 are similar to total BRS scoresfound in a European cohort of 437 children b32 weeks gestational agein which 18% of children who did not have severe disabilities scorednon-optimal in Orientation/Engagement and 13% scored non-optimalin Emotional Regulation. That study did not assess associations betweenBRS outcomes and maternal, perinatal, or NICU characteristics [21].
In a cohort of 20 low birthweight preterm infants (mean gestationalage of 29 weeks, no Grade III or IV IVH) evaluated at 6 months, half theinfants had total BRS scores in the lowest quartile for both Orientation/Engagement and Emotional Regulation, a rate that is higher than that ofthe ELGAN cohort at age 2 years [32]. Of the 57 premature infants in theBSID-II standardization sample, 32% scored non-optimal in EmotionalRegulation [17].
In amulticenter trial, 539 toddlers born at ELBW (mean birthweight792 g, mean gestational age 26 weeks) were evaluated at 18 and30 months using the BRS and BSID-II. In this cohort, BRS total and factorscores at 18 months were better predictors of Mental andMotor scoresat 30 months compared to earlier performance on Mental and Motorscales [22].
4.4. Strengths and limitations
4.4.1. Our study has several strengthsFirst, the large number of infants reduces the probability that we have
missed important associations, or claimed associations that might reflectthe instability of small numbers. Second, we selected infants based ongestational age and not birth weight. This minimizes inferential errorsrelated to factors associated with fetal growth restriction [33]. Third, wecollected all of our data prospectively. Fourth, examiners were notaware of the medical histories of the children they examined, therebyminimizing “diagnostic suspicion bias” [34]. Fifth, we haveminimized ob-server variability as best we can in the interpretation of ultrasound scans[15] and assessments of neurodevelopmental functions [19]. Sixth,attrition among survivors in the first two years was modest, with infor-mation about the two-year assessment available from 83% (for headcircumference).
4.4.2. Our study has a few limitationsFirst, we are extrapolating the child's performance on the BRS to the
child's behavior outside the test situation. The BRS measures the child'sbehavior only during a testing evaluationwhich is a potentially stressfulsituation for parent and child. Second, the BRS does not assess theparent's perception of the child's social–emotional development.Third, the BSID examiner was aware of the child's performance on theMDI and PDI, which could have influenced the subjective assessmentof the infant's behavior. Fourth, the scoring of the BRSwas not standard-ized across sites.
It will be important to determine if children with delays inorientation/engagement and emotional regulation continue to experi-ence challenges in social interaction and executive function in elementaryschool. Parenting style [35,36], maternal mental health [37], and childtemperament might also play an important role in the child's futuresocial–emotional development.
4.5. Implications
Over a quarter of extremely preterm infants in our study had relativeimpairments of engagement and emotional regulation. Our finding that≥15% of children who had an MDI of 85 or higher had non-optimal orquestionable scores on both BRS components we assessed supportsthe need for assessing social–emotional skills in early childhood, evenin children with normal motor and cognitive functioning.
Though quality of care recommendations for high risk premature in-fants recommend behavioral assessments [38,39], a recent survey of ac-ademic medical centers found that only 54% included a behavioralassessment in their NICU Follow Up Program [40]. Because social andemotional domains of child development have an impact on learning,executive function, and social competencies, assessment of these do-mains can inform decisions about interventions and supports for indi-vidual families and early childhood educators. Understanding theinfluence of limited engagement and emotional regulation skills couldinform practice guidelines used by those caring for survivors of extremeprematurity.
This studywas supportedby theNational Institute ofNeurological Dis-orders and Stroke through a cooperative agreement (5U01NS040069-05)and a grant (2R01NS040069-06A2), and by the National Institute ofChild Health and Human Development through a center grant award(5P30HD018655-28).
The authors gratefully acknowledge the contributions of their sub-jects, and their subjects' families, as well as those of their colleagues.
ELGAN study collaborators who made this report possible.Boston Children's Hospital, Boston, MAHaim Bassan, Samantha Butler, Adré Duplessis, Cecil Hahn, Catherine
Limperopoulos, Omar Khwaja, Janet S. SoulBaystate Medical Center, Springfield, MABhavesh Shah, Herbert Gilmore, Susan McQuistonBeth Israel Deaconess Medical Center, Boston, MACamilia R. MartinMassachusetts General Hospital, Boston, MARobert M. Insoft, Kalpathy KrishnamoorthyFloating Hospital for Children at Tufts Medical Center, Boston, MACynthia Cole, JohnM. Fiascone, Paige T. Church, Cecelia Keller, Karen
J. MillerU Mass Memorial Health Care, Worcester, MAFrancis Bednarek (deceased), Robin Adair, Richard Bream, AliceMill-
er, Albert Scheiner, Christy StineYale University School of Medicine, New Haven, CTRichard Ehrenkranz, Nancy Close, Elaine Romano, Joanne WilliamsWake Forest University Baptist Medical Center and Forsyth Medical
Center, Winston-Salem, NCT. Michael O'Shea, Deborah Allred, Robert Dillard, Don Goldstein,
Deborah Hiatt (deceased), Gail Hounshell, Ellen Waldrep, LisaWashburn, Cherrie D. Welch
University Health Systems of Eastern Carolina, Greenville, NCStephen C. Engelke, Sharon Buckwald, Rebecca Helms, Kathyrn
Kerkering, Scott S. MacGilvray, Peter ResnikNorth Carolina Children's Hospital, Chapel Hill, NCCarl Bose, Lisa Bostic, Diane Marshall, Kristi Milowic, Janice
WereszczakHelen DeVos Children's Hospital, Grand Rapids, MIMariel Poortenga, Wendy Burdo-Hartman, Lynn Fagerman, Kim
Lohr, Steve Pastyrnak, Dinah SuttonSparrow Hospital, Lansing, MI
930 L.A.C. Boyd et al. / Early Human Development 89 (2013) 925–930
Nicholas Olomu, Victoria J. Caine, Joan PriceMichigan State University, East Lansing, MINigel Paneth, Padmani KarnaUniversity of Chicago Medical Center, Chicago, ILMichael D. Schreiber, Leslie Caldarelli, Sunila E. O'Connor, Susan
Plesha-Troyke, Michael E. MsallWilliam Beaumont Hospital, Royal Oak, MIDaniel Batton, Karen Brooklier, Beth Kring, Melisa J. Oca, Katherine
M. Solomon
Conflict of interest
Among all authors there are no conflicts of interest.
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