Very preterm infants engage in an intervention to train their control of attention: results from the feasibility study of the Attention Control Training (ACT) randomised trial

Oliver Perra, Sam Wass, Alison McNulty, David Sweet, Kostas A Papageorgiou, Matthew Johnston, Delfina Bilello, Aaron Patterson, Fiona Alderdice, Oliver Perra, Sam Wass, Alison McNulty, David Sweet, Kostas A Papageorgiou, Matthew Johnston, Delfina Bilello, Aaron Patterson, Fiona Alderdice

Abstract

Background: Very premature birth (gestational age between 28 and 31 + 6 weeks) is associated with increased risk of cognitive delay and attention deficit disorder, which have been linked to anomalies in the development of executive functions (EFs) and their precursors. In particular, very preterm (VP) infants display anomalies in controlling attention and gathering task-relevant information. Early interventions that support attention control may be pivotal in providing a secure base for VP children's later attainments. The Attention Control Training (ACT) is a cognitive training intervention that targets infants' abilities to select visual information according to varying task demands but had not been tested in VP infants. We conducted a feasibility study to test the processes we intend to use in a trial delivering the ACT to VP infants.

Methods and design: We tested recruitment and retention of VP infants and their families in a randomised trial, as well as acceptability and completion of baseline and outcome measures. To evaluate these aims, we used descriptive quantitative statistics and qualitative methods to analyse feedback from infants' caregivers. We also investigated the quality of eye-tracking data collected and indicators of infants' engagement in the training, using descriptive statistics.

Results: Twelve VP infants were recruited, and 10 (83%) completed the study. Participants' parents had high education attainment. The rate of completion of baseline and outcome measures was optimal. VP infants demonstrated engagement in the training, completing on average 84 min of training over three visits, and displaying improved performance during this training. Eye-tracking data quality was moderate, but this did not interfere with infants' engagement in the training.

Discussion: The results suggest the ACT can be delivered to VP infants. However, challenges remain in recruitment of numerous and diverse samples. We discuss strategies to overcome these challenges informed by results of this study.

Trial registration: Registered Registration ID: NCT03896490 . Retrospectively registered at Clinical Trials Protocol Registration and Results System ( clinicaltrials.gov ).

Keywords: Attention; Computerised cognitive training; Eye-tracking methodology; Feasibility study; Infant; Premature.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
CONSORT diagram
Fig. 2
Fig. 2
Age (in months) at pre- and post-test of participants. Each row represents a participant, with triangles indicating the age at pre-test and the squares representing the age at post-test. The dashed line represents the threshold of 13 months of age, within which we had intended to run participants’ pre-test. Note: Participants are ordered by ID numbers, which were random-generated and do not reflect their order of inclusion in the study
Fig. 3
Fig. 3
Boxplots of task duration in the intervention group (n = 5) over training sessions. a Boxplots of complete and incomplete tasks. b Boxplots for completed tasks only (i.e. those lasting at least 240 s). Legend: Goal maint. = goal maintenance tasks; STM = short-term memory tasks. The line inside the box represents the median duration (in seconds), while the boxes represent the values between the 25th and 75th percentile. The whiskers represent the lowest and highest adjacent values. The red line in the graph represents 240 s, which was the criterion for deeming a training task complete. Goal maintenance #1: ‘Fly me’ task; Goal maintenance #2: ‘Butterfly’ task; STM #1: ‘Puzzle Memory’ task; STM #2: ‘Windows’ task; STM #3: ‘Tausendfuss’ task; STM #4: ‘Three Little Maids’ task; Target search #1: ‘Stars’ task; Target search #2: ‘Usual Suspects’ task; Target search #3: ‘Disengagement’ task
Fig. 4
Fig. 4
Performance in the three types of games by visit. The dashed lines represent average across all infants in the training group, while the full lines represent participants’ individual averages
Fig. 5
Fig. 5
Parent’s responses to questions on obstacles to participation by group allocation

References

    1. Aarnoudse-Moens CSH, Weisglas-Kuperus N, van Goudoever JB, Oosterlaan J. Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics. 2009;124(2):717–728. doi: 10.1542/peds.2008-2816.
    1. Ahlsson F, Kaijser M, Adami J, Lundgren M, Palme M. School performance after preterm birth. Epidemiology. 2015;26(1):106–111. doi: 10.1097/EDE.0000000000000171.
    1. Anderson P. Assessment and development of executive function (EF) during childhood. Child neuropsychology. 2002:8(2);71–82.
    1. Anderson PJ, Lee KJ, Roberts G, Spencer-Smith MM, Thompson DK, Seal ML, et al. Long-term academic functioning following Cogmed Working Memory Training for children born extremely preterm: a randomized controlled trial. J Pediatr. 2018;202:92-+. doi: 10.1016/j.jpeds.2018.07.003.
    1. Arpi E, Ferrari F. Preterm birth and behaviour problems in infants and preschool-age children: a review of the recent literature. Dev Med Child Neurol. 2013;55(9):788–796. doi: 10.1111/dmcn.12142.
    1. Ballieux H, Wass SV, Tomalski P, Kushnerenko E, Karmiloff-Smith A, Johnson MH, Moore DG. Applying gaze-contingent training within community settings to infants from diverse SES backgrounds. J Appl Dev Psychol. 2016;43:8–17. doi: 10.1016/j.appdev.2015.12.005.
    1. Barfield WD. Public health implications of very preterm birth. Clin Perinatol. 2018:45(3):565–77.
    1. Bayless S, Stevenson J. Executive functions in school-age children born very prematurely. Early Hum Dev. 2007;83(4):247–254. doi: 10.1016/j.earlhumdev.2006.05.021.
    1. Beck S, Wojdyla D, Say L, Betran AP, Merialdi M, Requejo JH, et al. The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ. 2010;88(1):31–38. doi: 10.2471/BLT.08.062554.
    1. Blencowe H, Cousens S, Chou D, Oestergaard M, Say L, Moller AB, Kinney M. Born too soon: the global epidemiology of 15 million preterm births understanding the data preterm birth ­­ what is it? Defining Preterm Birth. 2013;10(Suppl 1):1–13.
    1. Bonet M, Smith LK, Pilkington H, Draper ES, Zeitlin J. Neighbourhood deprivation and very preterm birth in an English and French cohort. BMC Pregnancy Childbirth. 2013;13(1):1–9.
    1. Bonevski B, Randell M, Paul C, Chapman K, Twyman L, Bryant J, Brozek I, Hughes C. Reaching the hard-to-reach: a systematic review of strategies for improving health and medical research with socially disadvantaged groups. BMC Med Res Methodol. 2014; 10.1186/1471-2288-14-42.
    1. Bonnier C. Evaluation of early stimulation programs for enhancing brain development. Acta Paediatr. 2008;97(7):853–8.
    1. Bora S, Pritchard VE, Moor S, Austin NC, Woodward LJ. Emotional and behavioural adjustment of children born very preterm at early school age. J Paediatr Child Health. 2011;47(12):863–869. doi: 10.1111/j.1440-1754.2011.02105.x.
    1. Breeman LD, Jaekel J, Baumann N, Bartmann P, Wolke D. Attention problems in very preterm children from childhood to adulthood: The Bavarian Longitudinal Study (vol 57, pg 132, 2016) J Child Psychol Psychiatry. 2016;57(6):E1.
    1. Broring T, Oostrom KJ, van Dijk-Lokkart EM, Lafeber HN, Brugman A, Oosterlaan J. Attention deficit hyperactivity disorder and autism spectrum disorder symptoms in school-age children born very preterm. Res Dev Disabil. 2018;74:103–112. doi: 10.1016/j.ridd.2018.01.001.
    1. Brydges CR, Landes JK, Reid CL, Campbell C, French N, Anderson M. Cognitive outcomes in children and adolescents born very preterm: a meta-analysis. Dev Med Child Neurol. 2018;60(5):452–468. doi: 10.1111/dmcn.13685.
    1. Cassiano RGM, Provenzi L, Linhares MBM, Gaspardo CM, Montirosso R. Maternal sociodemographic factors differentially affect the risk of behavioral problems in Brazilian and Italian preterm toddlers. Infant Behav Dev. 2018;50:165–173. doi: 10.1016/j.infbeh.2017.12.006.
    1. Cocks K, Torgerson DJ. Sample size calculations for pilot randomized trials: a confidence interval approach. J Clin Epidemiol. 2013;66(2):197–201. doi: 10.1016/j.jclinepi.2012.09.002.
    1. Davis L, Edwards H, Mohay H, Wollin J. The impact of very premature birth on the psychological health of mothers. Early Hum Dev. 2003;73(1-2):61–70.
    1. Delnord M, Hindori‐Mohangoo AD, Smith LK, Szamotulska K, Richards J.L, Deb‐Rinker P, Macfarlane A. Variations in very preterm birth rates in 30 high‐income countries: are valid international comparisons possible using routine data?. BJOG: An International Journal of Obstetrics & Gynaecology. 2017;124(5):785–94.
    1. Delobel-Ayoub M, Arnaud C, White-Koning M, Casper C, Pierrat V, Garel M, et al. Behavioral problems and cognitive performance at 5 years of age after very preterm birth: The EPIPAGE Study. Pediatrics. 2009;123(6):1485–1492. doi: 10.1542/peds.2008-1216.
    1. Diamond A. Executive functions. Annu Rev Psychol. 2013;64(1):135–168. doi: 10.1146/annurev-psych-113011-143750.
    1. Doebel S. Rethinking executive function and its development. Perspect Psychol Sci. 2020;15(4):942–956. doi: 10.1177/1745691620904771.
    1. Downes M, Kelly D, Day K, Marlow N, de Haan M. Visual attention control differences in 12-month-old preterm infants. Infant Behav Dev. 2018;50:180–188. doi: 10.1016/j.infbeh.2018.01.002.
    1. Ellard-Gray A, Jeffrey N, Choubak M, Crann S. Finding the hidden participant: solutions for recruiting hidden, hard-to-reach, and vulnerable populations. Int J Qual Methods. 2015;14(5):160940691562142. doi: 10.1177/1609406915621420.
    1. Eryigit-Madzwamuse S, Wolke D. Attention problems in relation to gestational age at birth and smallness for gestational age. Early Hum Dev. 2015;91(2):131–138. doi: 10.1016/j.earlhumdev.2015.01.004.
    1. Forssman L, Wass SV. Training basic visual attention leads to changes in responsiveness to social‐communicative cues in 9‐month‐olds. Child Dev. 2018;89(3):e199–213.
    1. Foulder-Hughes LA, Cooke RWI. Motor, cognitive, and behavioural disorders in children born very preterm. Dev Med Child Neurol. 2003;45(2):97–103. doi: 10.1111/j.1469-8749.2003.tb00912.x.
    1. Franz AP, Bolat GU, Bolat H, Matijasevich A, Santos IS, Silveira RC, Procianoy RS, Rohde LA, Moreira-Maia CR. Attention-deficit/hyperactivity disorder and very preterm/very low birth weight: a meta-analysis. Pediatrics. 2018;141(1):e20171645. doi: 10.1542/peds.2017-1645.
    1. Gagne JR, Van Hulle CA, Aksan N, Essex MJ, Goldsmith HH. Deriving childhood temperament measures from emotion-eliciting behavioral episodes: scale construction and initial validation. Psychol Assess. 2011;23(2):337–353. doi: 10.1037/a0021746.
    1. Gnigler M, Neubauer V, Griesmaier E, Zotter S, Kager K, Kiechl-Kohlendorfer U. Very preterm children are at increased risk of reduced processing speed at 5 years of age, predicted by typical complications of prematurity and prenatal smoking. Acta Paediatr. 2015;104(3):E124–E129. doi: 10.1111/apa.12859.
    1. Hendry A, Jones EJ, Charman T. Executive function in the first three years of life: Precursors, predictors and patterns. Dev Rev. 2016;42:1–33.
    1. Hirvonen M, Ojala R, Korhonen P, Haataja P, Eriksson K, Rantanen K, Gissler M, Luukkaala T, Tammela O. Intellectual disability in children aged less than seven years born moderately and late preterm compared with very preterm and term-born children - a nationwide birth cohort study. J Intellect Disabil Res. 2017;61(11):1034–1054. doi: 10.1111/jir.12394.
    1. Imafuku M, Kawai M, Niwa F, Shinya Y, Inagawa M, Myowa-Yamakoshi M. Preference for dynamic human images and gaze-following abilities in preterm infants at 6 and 12 months of age: an eye-tracking study. Infancy. 2017;22(2):223–239. doi: 10.1111/infa.12144.
    1. Jaekel J, Baumann N, Wolke D. Effects of gestational age at birth on cognitive performance: a function of cognitive workload demands. PLoS One. 2013;8(5):e65219. doi: 10.1371/journal.pone.0065219.
    1. Jaekel J, Bartmann P, Schneider W, Wolke D. Neurodevelopmental pathways to preterm children’s specific and general mathematic abilities. Early Hum Dev. 2014;90(10):639–644. doi: 10.1016/j.earlhumdev.2014.07.015.
    1. Johnson S, Wolke D, Hennessy E, Marlow N. Educational outcomes in extremely preterm children: neuropsychological correlates and predictors of attainment. Dev Neuropsychol. 2011;36(1):74–95. doi: 10.1080/87565641.2011.540541.
    1. Korzeniewski SJ. Relationships among gestational age and birthweight with cognitive deficits in children and adolescents born very preterm. Dev Med Child Neurol. 2018;60(5):436. doi: 10.1111/dmcn.13716.
    1. Langerock N, de Jonge L, van H. Graz MB, Hueppi PS, Tolsa CB, Barisnikov K. Emotional reactivity at 12 months in very preterm infants born at < 29 weeks of gestation. Infant Behav Dev. 2013;36(3):289–297. doi: 10.1016/j.infbeh.2013.02.006.
    1. Lawson KR, Ruff HA. Early focused attention predicts outcome for children born prematurely. J Dev Behav Pediatr. 2004;25(6):399–406. doi: 10.1097/00004703-200412000-00003.
    1. Linsell L, Malouf R, Johnson S, Morris J, Kurinczuk JJ, Marlow N. Prognostic factors for behavioral problems and psychiatric disorders in children born very preterm or very low birth weight: a systematic review. J Dev Behav Pediatr. 2016;37(1):88–102. doi: 10.1097/DBP.0000000000000238.
    1. Moiseev A, Doesburg SM, Herdman AT, Ribary U, Grunau RE. Altered network oscillations and functional connectivity dynamics in children born very preterm. Brain Topogr. 2015;28(5):726–745. doi: 10.1007/s10548-014-0416-0.
    1. Mullen EM. Mullen Scales of Early Learning: AGS Edition: American Guidance Services, Inc; 1995. 10.1002/9780470373699.speced1402
    1. Mundy P, Delgado C, Block J, Venezia M, Hogan A, Seibert J. A manual for the abridged early social communication scales. Coral Gables: University of Miami; 2003.
    1. Nosarti C, Giouroukou E, Micali N, Rifkin L, Morris RG, Murray RM. Impaired executive functioning in young adults born very preterm. J Int Neuropsychol Soc. 2007;13(4):571–581. doi: 10.1017/S1355617707070725.
    1. Ochiai M, Ichiyama M, Iwayarna M, Sakai Y, Yoshida K, Hara T. Longitudinal study of very low birth weight infants until 9 years of age; attention deficit hyperactivity and autistic features are correlated with their cognitive functions. Early Hum Dev. 2015;91(12):783–786. doi: 10.1016/j.earlhumdev.2015.09.005.
    1. Office for National Statistics. Birth characteristics in England and Wales. London: Office for National Stastics; 2017. .
    1. Pascal A, Govaert P, Oostra A, Naulaers G, Ortibus E, den Broeck C. Neurodevelopmental outcome in very preterm and very-low-birthweight infants born over the past decade: a meta-analytic review. Dev Med Child Neurol. 2018;60(4):342–355. doi: 10.1111/dmcn.13675.
    1. Perra O, Wass S, McNulty A, Sweet D, Papageorgiou K, Johnston M, Patterson A, Bilello D, Alderdice F. Training attention control of very preterm infants: protocol for a feasibility study of the Attention Control Training (ACT) Pilot Feasibility Stud. 2020;6(1):17. doi: 10.1186/s40814-020-0556-9.
    1. Planalp EM, Van Hulle C, Gagne JR, Hill Goldsmith H. The infant version of the laboratory temperament assessment battery (Lab-TAB): measurement properties and implications for concepts of temperament. Front Psychol. 2017;8. 10.3389/fpsyg.2017.00846.
    1. Putnam SP, Helbig AL, Gartstein MA, Rothbart MK, Leerkes E. Development and assessment of short and very short forms of the infant behavior questionnaire-revised. J Pers Assess. 2014;96(4):445–458. doi: 10.1080/00223891.2013.841171.
    1. Reuner G, Weinschenk A, Pauen S, Pietz J. Cognitive development in 7-to 24-month-old extremely/very-to-moderately/late preterm and full-term born infants: the mediating role of focused attention. Child Neuropsychol. 2015;21(3):314–330. doi: 10.1080/09297049.2014.899571.
    1. Rose SA, Feldman JF, Jankowski JJ. Modeling a cascade of effects: the role of speed and executive functioning in preterm/full-term differences in academic achievement. Dev Sci. 2011;14(5):1161–1175. doi: 10.1111/j.1467-7687.2011.01068.x.
    1. Rose SA, Feldman JF, Jankowski JJ, Van Rossem R. Basic information processing abilities at 11 years account for deficits in IQ associated with preterm birth. Intelligence. 2011;39(4):198–209. doi: 10.1016/j.intell.2011.03.003.
    1. Rose SA, Feldman JF, Jankowski JJ. Processing speed in the 1st year of life: a longitudinal study of preterm and full-term infants. Dev Psychol. 2002;38(6):895.
    1. Rose SA, Feldman JF, Jankowski JJ. Infant visual recognition memory: independent contributions of speed and attention. Dev Psychol. 2003;39(3):563.
    1. Rose SA, Feldman JF, Jankowski JJ. Information processing in toddlers: Continuity from infancy and persistence of preterm deficits. Intelligence. 2009;37(3):311–20.
    1. Ryu H, Han G, Choi J, Park H-K, Kim MJ, Ahn D-H, Lee HJ. Object permanence and the development of attention capacity in preterm and term infants: an eye-tracking study. Ital J Pediatr. 2017;43(1):90. doi: 10.1186/s13052-017-0408-2.
    1. Schieve LA, Tian LH, Rankin K, Kogan MD, Yeargin-Allsopp M, Visser S, Rosenberg D. Population impact of preterm birth and low birth weight on developmental disabilities in US children. Ann Epidemiol. 2016;26(4):267–274. doi: 10.1016/j.annepidem.2016.02.012.
    1. Scionti N, Cavallero M, Zogmaister C, Marzocchi GM. Is cognitive training effective for improving executive functions in preschoolers? A systematic review and meta-analysis. Front Psychol. 2020;10 10.3389/fpsyg.2019.02812.
    1. Shah PE, Robbins N, Coelho RB, Poehlmann J. The paradox of prematurity: The behavioral vulnerability of late preterm infants and the cognitive susceptibility of very preterm infants at 36 months post-term. Infant Behav Dev. 2013;36(1):50–62. doi: 10.1016/j.infbeh.2012.11.003.
    1. Smith LK, Draper ES, Manktelow BN, Dorling JS, Field DJ. Socioeconomic inequalities in very preterm birth rates. Archives of Disease in Childhood-Fetal and Neonatal Edition. 2007;92(1):F11–4.
    1. Spittle A, Orton J, Anderson PJ, Boyd R, Doyle LW. Early developmental intervention programmes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants. Cochrane Database Syst Rev. 2015;(11):CD005495 10.1002/14651858.CD005495.pub4.
    1. StataCorp . Stata Statistical Software: Release 13. 2015.
    1. Sun J, Mohay H, O’Callaghan M. A comparison of executive function in very preterm and term infants at 8 months corrected age. Early Hum Dev. 2009;85(4):225–230. doi: 10.1016/j.earlhumdev.2008.10.005.
    1. Telford EJ, Fletcher-Watson S, Gillespie-Smith K, Pataky R, Sparrow S, Murray IC, O'Hare A, Boardman JP. Preterm birth is associated with atypical social orienting in infancy detected using eye tracking. J Child Psychol Psychiatry. 2016;57(7):861–868. doi: 10.1111/jcpp.12546.
    1. Topolovec-Vranic J, Natarajan K. The use of social media in recruitment for medical research studies: a scoping review. J Med Internet Res. 2016;18(11):e286. doi: 10.2196/jmir.5698.
    1. Treyvaud K. Parent and family outcomes following very preterm or very low birth weight birth: a review. Semin Fetal Neonatal Med. 2014;19(2):131–135. doi: 10.1016/j.siny.2013.10.008.
    1. Treyvaud K, Lee KJ, Doyle LW, Anderson PJ. Very preterm birth influences parental mental health and family outcomes seven years after birth. J Pediatr. 2014;164(3):515–21.
    1. Twilhaar ES, Wade RM, de Kieviet JF, van Goudoever JB, van Elburg RM, Oosterlaan J. Cognitive outcomes of children born extremely or very preterm since the 1990s and associated risk factors a meta-analysis and meta-regression. JAMA Pediatr. 2018;172(4):361–367. doi: 10.1001/jamapediatrics.2017.5323.
    1. van Houdt CA, Van Wassenaer-Leemhuis AG, Oosterlaan J, Konigs M, Koopman-Esseboom C, Laarman ARC, et al. Executive function training in very preterm children: a randomized controlled trial. Eur Child Adolesc Psychiatry. 2020; 10.1007/s00787-020-01561-0.
    1. Wass S. Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn. 2011;75(1):18–28. doi: 10.1016/j.bandc.2010.10.005.
    1. Wass S, Porayska-Pomsta K, Johnson MH. Training attentional control in infancy. Curr Biol. 2011;21(18):1543–1547. doi: 10.1016/j.cub.2011.08.004.
    1. Wass SV. Applying cognitive training to target executive functions during early development. Child Neuropsychol. 2015;21(2):150–166. doi: 10.1080/09297049.2014.882888.
    1. Wass SV, Cook C, Clackson K. Changes in behavior and salivary cortisol after targeted cognitive training in typical 12-month-old infants. Dev Psychol. 2017;53(5):815.
    1. Wass SV, Forssman L, Leppanen J. Robustness and precision: how data quality may influence key dependent variables in infant eye-tracker analyses. Infancy. 2014;19(5):427–460. doi: 10.1111/infa.12055.
    1. Wass SV, Scerif G, Johnson MH. Training attentional control and working memory–Is younger, better?. Dev Rev. 20012;32(4):360–87.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe