Growing up after extremely preterm birth

e Lo

the lmecenunndin thons

Extremely preterm (EP) births, beforelenge, minrough aother peir famerabiliio-econment w

Mental health outcomes are generally evaluated as part of lon-gitudinal studies which have, for the most part, sought to identify

the prevalence of disorders at various ages. Like all outcome

anage, but groupse representative ofby the simple factore contemporarydren making com-en studying out-erlying hypothesislistic estimates of

studying mental health disorders and to facilitate comparison be-tween studies, yet variation may still exist depending on themeasure used [6]. However, the often insurmountable economicand practical challenges of implementing diagnostic interviewsmean that most studies have relied solely on behavioural ques-tionnaires (see Johnson [7] and Arpi and Ferrari [8] for reviews).These typically generate higher rates of individuals that score above

* Corresponding author. Address: Department of Health Sciences, University ofLeicester, 22e28 Princess Road West, Leicester LE1 6TP, UK. Tel.: 44 (0) 116 2525798; fax: 44 (0) 116 252 3272.

Contents lists availab

Seminars in Fetal &

.e

Seminars in Fetal & Neonatal Medicine 19 (2014) 97e104E-mail address: sjj19@le.ac.uk (S. Johnson).2. Studying mental health following extremely preterm birth group differences are computed.It is widely considered preferable to use diagnostic criteria forimpairments are themost frequent adverse outcomes [3,4], but thereis growing interest in the impact of preterm birth on mental healthand wellbeing. Here we review literature relating to mental healthoutcomes following EP birth. Although we focus on reports from themost contemporary cohorts, much may be gained through under-standing outcomes for older cohorts now in adult life.

Single centre studies are more practical to mof babies born in individual hospitals may not bthe wider population. Further challenges occurthat populations change over time, such that mcohorts comprise a higher proportion of EP chilparison with historical reports challenging. Whcomes it is important that there is a strong undand that pre-study power calculations using reaextendacross the lifespan.AlthoughEPbirths comprise just 0.6% of allbirths, morbidity is highest among these survivors [1,2]. Cognitive

Having due regard to these in drawing conclusions.

have a profound impact on developcontinue to pose the greatest chalProviding life-sustaining treatmentstressors and supporting the family thkey challenges for neonatologists andperinatal care. For these babies and thdoes not end there. The biological vulnwhich may be amplied through soc1744-165X/$ e see front matter 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.siny.2013.11.00428 weeks of gestation,for neonatal medicine.imising environmentaltraumatic life event arerofessionals involved inilies, however, the carety conferred by EP birth,omic disadvantage, canith consequences that

studies, these suffer the inherent problems of selective drop-out.Some of the issues relating to the maintenance of cohorts haverecently been discussed [5]. Key aspects of cohort evaluations are:

Having a clear denominator in order to evaluate how the nd-ings may be extrapolated to other studies and how represen-tative they are of the population from which they are drawn.

Evaluating the effect of drop-outs and, where necessary, sup-plementing the ndings with sensitivity analyses or imputationtechniques.1. Introductionoutcomes

Samantha Johnson a,*, Neil Marlow b

aDepartment of Health Sciences, University of Leicester, Leicester LE1 6TP, UKbDepartment of Academic Neonatology, Institute for Womens Health, University Colleg

Keywords:Attention decit hyperactivity disorderAutism spectrum disordersComorbidityMental healthOutcomesPreterm birth

s u m m a r y

There is growing interest inreview literature relating toyears, school age and adolesfor inattention, socio-commpreterm. Both behavioural aformental health disordersmethodological consideratiReview

journal homepage: wwwAll rights reserved.: Lifespan mental health

ndon, London, UK

ong-termmentalhealth sequelaeof extremely pretermbirth. In thispaperwental health outcomes across the lifespan. Studies conducted in the preschoolce, and adulthood showcontinuity in outcomes and point to an increased riskicative problems and emotional difculties in individuals born extremelyneuroimaging studies also provide evidence of a neurodevelopmental originis population. Herewe summarise contemporary evidence and highlight keyfor carrying out and interpreting studies in this eld.

2013 Elsevier Ltd. All rights reserved.

le at ScienceDirect

Neonatal Medicine

lsevier .com/locate/s iny

the cut-off for clinically signicant problems than meet the criteriafor disorders. This is illustrated using data from the UK EPICureStudy (Fig. 1) [9]. As part of a follow-up at 11 years of age,emotional, conduct, hyperactivity/inattention and peer relation-ship problems in a cohort of children born EP (

Table 1Prospective studies of behavioural and emotional problems and psychiatric disorders in extremely low birthweight (ELBW) or extremely preterm (EP) preschoolers born in the1990s and beyonda.

Publication Sample characteristics Domains with signicantly highermean scores in EP/ELBW children

Measure

Age (years) Birth year Preterm Control

Clark et al. [48] 2 1998e2001 N 39 N 103 Regulation BRSSingle centre

health [57]. In EP children, internalising behaviour problems at 2.5years were a signicant predictor of disorders at 11 years of age,whereas externalising difculties were not [10]. Scores on the CBCLWithdrawn subscale have also been shown to be a signicantpredictor of later ASD symptoms [25], and scores on this and theEmotionally Reactive subscale have also been associated withpositive M-CHAT screens [58]. Using a VP sample, Treyvaud et al.[59] have also shown that internalising difculties, socialeemotional competence and externalising problems at 2 years pre-dicted emotional symptoms, peer problems and conduct problemsat 5 years, respectively. Socialeemotional problems at age 5 yearsalso predicted psychiatric disorders at age 7 years [60]. With suchspecicity in prediction, it may be assumed that there is stability inoutcomes among EP children and that the early problems high-lighted above will manifest in attention, emotional problems andASD later in childhood.

preterm children [68]. Three studies of EP/ELBW children reportconsistently elevated risks for disorders with prevalence estimatesranging 23e32% [10,24,60]. These also provide evidence for thespecic risk for attention and social problems in this population(Table 3) [10,24]. In their VP cohort, Treyvaud et al. [60] did notreport a signicant increase in these disorders which the authorsacknowledge may be a result of low statistical power; however,there was a trend for a higher rate of ADHD and anxiety disorders.Thus there appears to be a pattern of elevated risk for symptomsand disorders associated with ADHD, peer relationship problemsand emotional disorders, the cluster of which has been termed thepreterm behavioural phenotype [26].

The symptoms and correlates of ADHD and ASD in EP childrenmay indicate a different aetiology that is associated with aberrantbrain development. Indeed, Laucht et al. [29] have shown thatpsychosocial and biological risk factors had independent effects on

low

ntro

11

65

17

15

S. Johnson, N. Marlow / Seminars in Fetal & Neonatal Medicine 19 (2014) 97e1041004. School age and adolescence

4.1. Dimensional studies

EP survivors are at high risk for clinically signicant problemsthroughout middle childhood, with prevalence estimates of 18e38% [24,26,61e63]. Studies have also shown that the mental healthproblems of EP children have a greater impact on their daily livingthan those of term-born controls [62,64]. Commensurate with thetemporal stability in neurodevelopmental outcomes [65], the rateof mental health problems remains high despite advances inneonatal care [61,64]. Whereas there is a greater risk for behaviourproblems in EP versus VP children [3,66], there is little evidence fora gestation-related gradient within the EP group itself [62,64].

Compared with the preschool years, there is greater consistencyin ndings at school age. In three studies of six EP/ELBW cohorts,the authors identied an excess of attention, social and thought oremotional problems despite using different measures [61,64,67]. Ina study using multi-informant data to identify pervasive problems,EP children had signicantly more problems on all scales but oddsratios (ORs) were greatest for these three domains [62]. Conradet al. [14] also found that only depression/anxiety and hyperactiv-ity/inattention were signicantly increased in ELBW children aged7e16 years. These ndings thus point to a cluster of attention, socialand emotional problems in EP children [26].

4.2. Diagnostic studies

In a recent meta-analysis of ve studies [68], the authors re-ported a weighted OR of 3.66 for psychiatric disorders among

Table 3Mental health disorders in children born extremely preterm (EP) or with extremely

Publication Sample characteristics

Age (years) Birth year Preterm Co

Scott et al. [49] 5 2001e2003 N 148 NSingle centre

bipolar affective disorder in adults born

born extremely low birth weight or very preterm in the 1990s. JAMA2003;289:3264e72.

[4] Johnson S, Fawke J, Hennessy E, Rowell V, Thomas S, Wolke D, et al.Neurodevelopmental disability through 11 years in children born before26 weeks of gestation: the EPICure study. Pediatrics 2009;124:e249e57.

[5] Marlow N. Measuring neurodevelopmental outcome in neonatal trials: acontinuing and increasing challenge. Arch Dis Child Fetal Neonatal Ed2013;98:F554e8.

[6] Angold A, Erkanli A, Copeland W, Goodman R, Fisher PW, Costello EJ.Psychiatric diagnostic interviews for children and adolescents: acomparative study. J Am Acad Child Adolesc Psychiatry 2012;51:506e17.

[7] Johnson S. Cognitive and behavioural outcomes following very pretermbirth. Semin Fetal Neonatal Med 2007;12:363e73.

[8] Arpi E, Ferrari F. Preterm birth and behaviour problems in infants andpreschool-age children: a review of the recent literature. Dev Med ChildNeurol 2013;55:788e96.

[9] EPICure Studies. Population based studies of survival and later healthstatus in extremely premature infants. www.epicure.ac.uk; 2013.

*[10] Johnson S, Hollis C, Kochhar P, Hennessy E, Wolke D, Marlow N. Psychiatricdisorders in extremely preterm children: longitudinal nding at age 11years in the EPICure study. J Am Acad Child Adolesc Psychiatry 2010;49.453.e1e463.e1.

[11] Bora S, Pritchard VE, Moor S, Austin NC, Woodward LJ. Emotional andbehavioural adjustment of children born very preterm at early school age.J Paediatr Child Health 2011;47:863e9.

[12] Dahl LB, Kaaresen PI, Tunby J, Handegard BH, Kvernmo S, Ronning JA.Emotional, behavioral, social, and academic outcomes in adolescents bornwith very low birth weight. Pediatrics 2006;118:E449e59.

[13] van Dulmen MHM, Egeland B. Analyzing multiple informant data on childand adolescent behavior problems: predictive validity and comparison ofaggregation procedures. Int J Behav Dev 2011;35:84e92.

[14] Conrad AL, Richman L, Lindgren S, Nopoulos P. Biological and environ-

al &term, the societal consequences of EP birth in young adulthoodappear to be somewhat less than anticipated, with better socialadaptation and quality of life than might once have beenpredicted.

6. A biological basis for psychiatric morbidity

A biological basis for psychiatric disorders in EP survivors isperhaps understandable after consideration of the effect of pre-maturity on brain development, which has been described as acomplex amalgam of destructive and developmental inuences[90]. Studies using magnetic resonance imaging and computationaltechniques have identied differences in the brains of EP childrenand adults which may act as biomarkers for these evolving condi-tions [91]. These include not only ongoing adaptation to destructivelesions, but more subtle differences in brain size/surface area [92]and regional volumes such as the frontal and temporal cortex orhippocampus [93], deep gray matter [94] and corpus callosum [95].Reduced complexity of brain folding and abnormalities on func-tional activation imply altered developmental trajectories thatmirror impaired executive functions [96]. As discussed above, suchcognitive decits may underpin mental health symptoms and dis-orders in EP children [77,97].

Although ex-preterm brain structure and function in relation tospecic psychiatric disorders have not been investigated in largepopulations of EP individuals, data from middle childhood sug-gests that structural alterations may be associated with behav-ioural ndings, for example with attention and internalisingbehaviours (fractional anisotropy in a range of overlappingareas),[98] socio-emotional development (hippocampal size) [99]and wellbeing (cerebellar growth) [100]. As yet, such studieshave not been sufciently large or systematic to develop a pictureof the underlying neural basis for psychiatric disorders associatedwith preterm birth, but the data suggest that there may be abiological basis for the clinically observed excess of psychopa-thology in this population.

7. Conclusions

Studies of mental health outcomes following EP birth havelargely sought to document the prevalence of disorders inmiddle childhood and adolescence, but reports of longer-termoutcomes are beginning to surface as contemporary cohortsreach adulthood. Early attention and regulatory problems areevident in the preschool years and, by childhood, the greaterspecicity in outcomes points to a cluster of inattention, peerrelationship problems and emotional symptoms. Approximately25% have psychiatric disorders but up to double those numbersmay have signicant difculties that impact on function. Thisbehavioural phenotype shows continuity into adult life withincreased risk for disorders, yet quality of life and social adap-tation are better than may have once been anticipated. Mentalhealth symptoms appear to have a strong neurodevelopmentalorigin which may be mediated by core cognitive decits asso-ciated with EP birth. Targeted screening for the cluster of mentalhealth problems associated with EP birth may be benecial fordetecting children with subclinical difculties, particularly dur-ing the preschool years when problems start to become evident.Future studies are needed to identify resilience and risk factorsfor mental health disorders and to further elucidate the role ofparental mental health in the evolution of psychopathology inEP children. As more EP children continue to enter society, agreater understanding of the aetiology and functional impact ofthese disorders will aid in providing appropriate lifelong

S. Johnson, N. Marlow / Seminars in Fet102support.Funding sources

Neil Marlow receives a proportion of funding from the Depart-ment of Healths NIHR Biomedical Research Centres fundingscheme at UCLH/UCL.

References

[1] Saigal S, Doyle L. An overview of mortality and sequelae of preterm birthfrom infancy to adulthood. Lancet 2008;371:261e9.

[2] MacKay DF, Smith GC, Dobbie R, Pell JP. Gestational age at delivery andspecial educational need: retrospective cohort study of 407,503 school-children. PLoS Med 2010;7:e1000289.

[3] Anderson P, Doyle LW. Neurobehavioral outcomes of school-age children

Practice points

Children born extremely preterm may have attention,emotional or peer relationship problems that do not meetdiagnostic criteria but which may impact on daily func-tion, for which intervention may be beneficial.

Screening for behaviour problems from 2 years of agemay aid in detecting children with early difficulties andthose at risk of later mental health disorders.

Researchers and clinicians should consider includingmental health assessments as part of neuro-developmental outcome evaluations.

Research directions

Longitudinal studies are needed to investigate the evo-lution of mental health sequelae throughout the lifespan.

The role of parental mental health in the development ofchildhood psychopathology requires elucidation in thispopulation.

More studies are required to understand the neurologicalbases of mental health disorders in extremely pretermchildren.

Neonatal Medicine 19 (2014) 97e104mental predictors of behavioral sequelae in children born preterm. Pedi-atrics 2010;125:e83e9.

tal &[15] Spiker D, Kraemer HC, Constantine NA, Bryant D. Reliability and validity ofbehavior problem checklists as measures of stable traits in low birthweight, premature preschoolers. Child Dev 1992;63:1481e96.

[16] Gardner F, Johnson A, Yudkin P, Bowler U, Hockley C, Mutch L, et al.Behavioral and emotional adjustment of teenagers in mainstream schoolwho were born before 29 weeks gestation. Pediatrics 2004;114:676e82.

[17] Saigal S, Pinelli J, Hoult L, Kim MM, Boyle M. Psychopathology and socialcompetencies of adolescents who were extremely low birth weight. Pe-diatrics 2003;111:969e75.

[18] Renk K. Cross-informant ratings of the behavior of children and adoles-cents: the gold standard. J Child Fam Stud 2005;14:457e68.

[19] Ford T, Goodman R, Meltzer H. The British child and adolescent mentalhealth survey 1999: the prevalence of DSM-IV disorders. J Am Acad ChildAdolesc Psychiatry 2003;42:1203e11.

[20] Hudziak JJ, Achenbach TM, Althoff RR, Pine DS. A dimensional approach todevelopmental psychopathology. Int J Methods Psychiatr Res2007;16(Suppl. 1):S16e23.

[21] Goodman A, Goodman R. Strengths and difculties questionnaire as adimensional measure of child mental health. J Am Acad Child AdolescPsychiatry 2009;48:400e3.

[22] Nigg JT. Future directions in ADHD etiology research. J Clin Child AdolescPsychol 2012;41:524e33.

[23] Coghill D, Sonuga-Barke EJ. Annual research review: categories versusdimensions in the classication and conceptualisation of child andadolescent mental disorders e implications of recent empirical study. JChild Psychol Psychiatry Allied Discipl 2012;53:469e89.

*[24] Hack M, Taylor HG, Schlichter M, Andreias L, Drotar D, Klein N. Behavioraloutcomes of extremely low birth weight children at age 8 years. J DevBehav Pediatr 2009;30:122e30.

[25] Johnson S, Hollis C, Kochhar P, Hennessy E, Wolke D, Marlow N. Autismspectrum disorders in extremely preterm children. J Pediatr 2010;156:525e31.

*[26] Johnson S, Marlow N. Preterm birth and childhood psychiatric disorders.Pediatr Res 2011;69:11re8r.

[27] Dennis M, Francis DJ, Cirino PT, Schachar R, Barnes MA, Fletcher JM. WhyIQ is not a covariate in cognitive studies of neurodevelopmental disorders.J Int Neuropsychol Soc 2009;15:331e43.

[28] Taylor HG. Children born preterm or with very low birth weight can haveboth global and selective cognitive decits. J Dev Behav Pediatr 2006;27:485e6. author reply 6e7.

[29] Laucht M, Esser G, Baving L, Gerhold M, Hoesch I, Ihle W, et al. Behavioralsequelae of perinatal insults and early family adversity at 8 years of age. JAm Acad Child Adolesc Psychiatry 2000;39:1229e37.

[30] Treyvaud K, Anderson VA, Lee KJ, Woodward LJ, Newnham C, Inder TE,et al. Parental mental health and early socialeemotional development ofchildren born very preterm. J Pediatr Psychol 2010;35:768e77.

[31] Miles MS, Holditch-Davis D, Schwartz TA, Scher M. Depressive symptomsin mothers of prematurely born infants. J Dev Behav Pediatr 2007;28:36e44.

[32] Glazebrook C, Marlow N, Israel C, Croudace T, Johnson S, White IR, et al.Randomised trial of a parenting intervention during neonatal intensivecare. Arch Dis Child Fetal Neonatal Ed 2007;92:F438e43.

[33] Indredavik MS, Vik T, Heyerdahl S, Kulseng S, Fayers P, Brubakk AM.Psychiatric symptoms and disorders in adolescents with low birth weight.Arch Dis Child 2004;89:F445e50.

[34] Botting N, Powls A, Cooke RWI, Marlow N. Attention decit hyperac-tivity disorders and other psychiatric outcomes in very low birthweightchildren at 12 years. J Child Psychol Psychiatry Allied Discipl 1997;38:931e41.

[35] Indredavik MS, Vik T, Evensen AI, Skranes J, Taraldsen G, Brubakk A.Perinatal risk and psychiatric outcome in adolescents born preterm withvery low birth weight or term small for gestational age. J Dev BehavPediatr 2010;31:286e94.

*[36] Spittle AJ, Treyvaud K, Doyle LW, Roberts G, Lee KJ, Inder TE, et al. Earlyemergence of behavior and socialeemotional problems in very preterminfants. J Am Acad Child Adolesc Psychiatry 2009;48:909e18.

[37] Huhtala M, Korja R, Lehtonen L, Haataja L, Lapinleimu H, Rautava P.Parental psychological well-being and behavioral outcome of very lowbirth weight infants at 3 years. Pediatrics 2012;129:e937e44.

[38] Jaekel J, Wolke D, Bartmann P. Poor attention rather than hyperactivity/impulsivity predicts academic achievement in very preterm and full-termadolescents. Psychol Med 2013;43:183e96.

[39] Jaekel J, Wolke D, Chernova J. Mother and child behaviour in very pretermand term dyads at 6 and 8 years. Dev Med Child Neurol 2012;54:716e23.

[40] Forcada-Guex M, Pierrehubert B, Borghini A, Moessinger A, Muller-Nix CM. Early dyadic patterns of mothereinfant interactions and out-comes of prematurity at 18 months. Pediatrics 2006;118:107e14.

[41] Assel M, Landry S, Swank P, Steelman L, Miller-Loncar C, Smith K. How domothers childrearing histories, stress and parenting affect childrensbehavioural outcomes? Child Care Health Dev 2002;28:359e68.

[42] Korja R, Latva R, Lehtonen L. The effects of preterm birth on motherein-fant interaction and attachment during the infants rst two years. ActaObstet Gynecol Scand 2012;91:164e73.

S. Johnson, N. Marlow / Seminars in Fe[43] Vanderbilt D, Gleason MM. Mental health concerns of the premature in-fant through the lifespan. Pediatr Clin North Am 2011;58:815e32.[44] ASEBA. Achenbach system of empirically based assessment. http://www.aseba.org/; 2012.

[45] Goodman R. The strengths and difculties questionnaire: a research note.J Child Psychol Psychiatry 1997;38:581e6.

[46] Woodward LJ, Moor S, Hood KM, Champion PR, Foster-Cohen S, Inder TE,et al. Very preterm children show impairments across multiple neuro-developmental domains by age 4 years. Archs Dis Childh Fetal NeonatalEd 2009;94:F339e44.

[47] Elgen SK, Leversen KT, Grundt JH, Hurum J, Sundby AB, Elgen IB, et al.Mental health at 5 years among children born extremely preterm: a na-tional population-based study. Eur Child Adolesc Psychiatry 2012;21:583e9.

[48] Clark CAC, Woodward LJ, Horwood LJ, Moor S. Development of emotionaland behavioral regulation in children born extremely preterm and verypreterm: biological and social inuences. Child Dev 2008;79:1444e62.

*[49] Scott MN, Taylor HG, Fristad MA, Klein N, Espy KA, Minich N, et al.Behavior disorders in extremely preterm/extremely low birth weightchildren in kindergarten. J Dev Behav Pediatr 2012;33:202e13.

[50] Kuban KCK, OShea TM, Allred EN, Tager-Flusberg H, Goldstein DJ,Leviton A. Positive screening on the Modied Checklist for Autism inToddlers (M-CHAT) in extremely low gestational age newborns. J Pediatr2009;154:535e40.

[51] Moore T, Johnson S, Hennessy E, Marlow N. Screening for autism inextremely preterm infants: problems in interpretation. Dev Med ChildNeurol 2012;54:514e20.

[52] Stephens BE, Bann CM, Watson VE, Sheinkopf SJ, Perata-Carcelen M,Bodnar A, et al. Screening for autism spectrum disorders in extremelypreterm infants. J Dev Behav Pediatr 2012;33:535e41.

[53] Johnson S, Marlow N. Positive screening results on the modied checklistfor autism in toddlers: implications for very preterm populations. J Pediatr2009;154:478e80.

[54] Luyster RJ, Kuban KCK, OShea TM, Paneth N, Aldred EN, Leviton A. Themodied checklist for autism in toddlers in extremely low gestational agenewborns: individual items associated with motor, cognitive, vision andhearing limitations. Paediatr Perinat Epidemiol 2011;25:366e76.

[55] Gray RF, Indurkhya A, McCormick MC. Prevalence, stability, and predictorsof clinically signicant behavior problems in low birth weight children at3, 5, and 8 years of age. Pediatrics 2004;114:736e43.

[56] Delobel-Ayoub M, Arnaud C, White-Koning M, Casper C, Pierrat V,Garel M, et al. Behavioral problems and cognitive performance at 5 yearsof age after very preterm birth: the EPIPAGE study. Pediatrics 2009;123:1485e92.

[57] Briggs-Gowan MJ, Carter AS. Socialeemotional screening status in earlychildhood predicts elementary school outcomes. Pediatrics 2008;121:957e62.

[58] Limperopoulos C, Bassan H, Sullivan NR, Soul JS, Robertson RL, Moore M,et al. Positive screening for autism in ex-preterm infants: prevalence andrisk factors. Pediatrics 2008;121:758e65.

[59] Treyvaud K, Doyle LW, Lee KJ, Roberts G, Lim J, Inder TE, et al. Socialeemotional difculties in very preterm and term 2 year olds predict specicsocialeemotional problems at the age of 5 years. J Pediatr Psychol2012;37:779e85.

[60] Treyvaud K, Ure A, Doyle LW, Lee KJ, Rogers CE, Kidokoro H, et al. Psy-chiatric outcomes at age seven for very preterm children: rates and pre-dictors. J Child Psychol Psychiatry Allied Discipl 2013;54:772e9.

[61] Farooqi A, Hagglof B, Sedin G, Gothefors L, Serenius F. Mental health andsocial competencies of 10- to 12-year-old children born at 23 to 25 weeksof gestation in the 1990s: a Swedish national prospective follow-up study.Pediatrics 2007;120:118e33.

[62] Samara M, Marlow N, Wolke D. Pervasive behavior problems at 6 years ofage in a total-population sample of children born at 25 weeks ofgestation. Pediatrics 2008;122:562e73.

[63] Grunau R, Whiteld MF, Fay TB. Psychosocial and academic characteristicsof extremely low birth weight (

[70] Linnet KM, Wisborg K, Agerbo E, Secher NJ, Thomsen PH, Henriksen TB.Gestational age, birth weight, and the risk of hyperkinetic disorder. ArchDis Child 2006;91:655e60.

*[71] Johnson S, Wolke D. Behavioural outcomes and psychopathology duringadolescence. Early Hum Dev 2013;89:199e207.

[72] Hack M, Flannery DJ, Schluchter M, Cartar L, Borawski E, Klein N. Out-comes in young adulthood for very-low-birth-weight infants. N Engl JMed 2002;346:149e57.

[73] Shum D, Neulinger K, OCallaghan M, Mohay H. Attentional problems inchildren born with very preterm or with extremely low birth weight at 7e9 years. Arch Clin Neuropsychol 2008;23:103e12.

[74] Martel MM, von Eye A, Nigg JT. Revisiting the latent structure of ADHD: isthere a g factor? J Child Psychol Psychiatry 2010;51:905e14.

[75] Mulder H, Pitchford NJ, Hagger MS, Marlow N. Development of executivefunction and attention in preterm children: a systematic review. DevNeuropsychol 2009;34:393e421.

[76] Aarnoudse-Moens CS, Duivenvoorden HJ, Weisglas-Kuperus N, VanGoudoever JB, Oosterlaan J. The prole of executive function in verypreterm children at 4 to 12 years. Dev Med Child Neurol 2012;54:247e53.

[77] Nadeau L, Boivin M, Tessier R, Lefebvre F, Robaey P. Mediators of behav-ioral problems in 7-year-old children born after 24 to 28 weeks ofgestation. J Dev Behav Pediatr 2001;22:1e10.

[78] Hack M, Youngstrom EA, Cartar L, Schluchter M, Taylor HG, Flannery D,et al. Behavioral outcomes and evidence of psychopathology among verylow birth weight infants at age 20 years. Pediatrics 2004;114:932e40.

[79] Skranes J, Vangberg TR, Kulseng S, Indredavik MS, Evensen KA,Martinussen M, et al. Clinical ndings and white matter abnormalitiesseen on diffusion tensor imaging in adolescents with very low birthweight. Brain 2007;130:654e66.

[80] American Psychiatric Association. Diagnostic and statistical manual ofmental disorders (DSM-V). 5th ed. Washington DC: APA; 2013.

[81] Moster D, Lie RT, Markestad T. Long-term medical and social conse-quences of preterm birth. N Engl J Med 2008;359:262e73.

[82] Halmoy A, Klungsoyr K, Skjaerven R, Haavik J. Pre- and perinatal riskfactors in adults with attention-decit/hyperactivity disorder. Biol Psy-chiatry 2012;71:474e81.

adulthood. Comparison with normal birth-weight controls. JAMA2006;295:667e75.

[87] Hallin AL, Stjernqvist K. Follow-up of adolescents born extremely pre-term: self-perceived mental health, social and relational outcomes. ActaPaediatr 2011;100:279e83.

[88] Cooke RW. Health, lifestyle, and quality of life for young adults born verypreterm. Archs Dis Childh 2004;89:201e6.

*[89] Burnett A, Davey CG, Wood SJ, Wilson-Ching M, Molloy C, Cheong JL, et al.Extremely preterm birth and adolescent mental health in a geographicalcohort born in the 1990s. Psychol Med 2013 Aug;28:1e12 [Epub ahead ofprint].

[90] Volpe JJ. Brain injury in premature infants: a complex amalgam ofdestructive and developmental disturbances. Lancet Neurol 2009;8:110e24.

[91] Ment LR, Hirtz D, Huppi PS. Imaging biomarkers of outcome in thedeveloping preterm brain. Lancet Neurol 2009;8:1042e55.

[92] Skranes J, Lohaugen GC, Martinussen M, Haberg A, Brubakk AM, Dale AM.Cortical surface area and IQ in very-low-birth-weight (VLBW) youngadults. Cortex 2013;49:2264e71.

[93] de Kieviet JF, Zoetebier L, van Elburg RM, Vermeulen RJ, Oosterlaan J. Braindevelopment of very preterm and very low-birthweight children inchildhood and adolescence: a meta-analysis. Dev Med Child Neurol2012;54:313e23.

[94] Boardman JP, Counsell SJ, Rueckert D, Kapellou O, Bhatia KK, Aljabar P,et al. Abnormal deep grey matter development following preterm birthdetected using deformation-based morphometry. Neuroimage 2006;32:70e8.

[95] Northam GB, Liegeois F, Tournier JD, Croft LJ, Johns PN, Chong WK, et al.Interhemispheric temporal lobe connectivity predicts language impair-ment in adolescents born preterm. Brain 2012;135:3781e98.

[96] Smyser CD, Snyder AZ, Shimony JS, Blazey TM, Inder TE, Neil JJ. Effects ofwhite matter injury on resting state FMRI measures in prematurely borninfants. PLoS One 2013;8:e68098.

[97] Mulder H, Pitchford NJ, Marlow N. Processing speed mediates executivefunction difculties in very preterm children in middle childhood. J IntNeuropsychol Soc 2011 Mar;28:1e10 [Epub ahead of print].

[98] Loe IM, Lee ES, Feldman HM. Attention and internalizing behaviors in

S. Johnson, N. Marlow / Seminars in Fetal & Neonatal Medicine 19 (2014) 97e104104*[83] Nosarti C, Reichenberg A, Murray RM, Cnattingius S, Lambe MP, Yin L, et al.Preterm birth and psychiatric disorders in young adult life. Arch GenPsychiatry 2012;69:E1e8.

[84] Lindstrom K, Lindblad F, Hjern A. Psychiatric morbidity in adolescents andyoung adults born preterm: a Swedish national cohort study. Pediatrics2009;123:e46e53.

[85] Crump C, Winkleby MA, Sundquist K, Sundquist J. Preterm birth andpsychiatric medication prescription in young adulthood: a Swedish na-tional cohort study. Int J Epidemiol 2010;39:1522e30.

*[86] Saigal S, Stoskopf B, Streiner DL, Boyle M, Pinelli J, Paneth N, et al. Tran-sition of extremely low-birth weight infants from adolescence to youngrelation to white matter in children born preterm. J Dev Behav Pediatr2013;34:156e64.

[99] Rogers CE, Anderson PJ, Thompson DK, Kidokoro H, Wallendorf M,Treyvaud K, et al. Regional cerebral development at term relates to school-age socialeemotional development in very preterm children. J Am AcadChild Adolesc Psychiatry 2012;51:181e91.

[100] Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung HY, Nosarti C, et al.Cerebellar growth and behavioural and neuropsychological outcome inpreterm adolescents. Brain 2008;131:1344e51.

Growing up after extremely preterm birth: Lifespan mental health outcomes1 Introduction2 Studying mental health following extremely preterm birth3 The preschool years3.1 Behaviour and emotional problems in the preschool years3.2 Early indicators of autism spectrum disorders (ASD)3.3 Predictive validity of early assessments

4 School age and adolescence4.1 Dimensional studies4.2 Diagnostic studies4.3 Attention deficit hyperactivity disorder4.4 Autism spectrum disorders4.5 Comorbidity

5 Mental health in adulthood6 A biological basis for psychiatric morbidity7 ConclusionsFunding sourcesReferences