Long-term motor outcomes of very preterm and/or very low birth weight individuals without cerebral palsy: A review of the current evidence

  • Kari Anne I. Evensen
    Correspondence
    Corresponding author. PO Box 8905, NO-7491, Trondheim, Norway.
    Affiliations
    Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway

    Department of Public Health and Nursing, Norwegian University of Science and Technology, Trondheim, Norway

    Unit for Physiotherapy Services, Trondheim Municipality, Trondheim, Norway

    Department of Physiotherapy, Oslo Metropolitan University, Oslo, Norway
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  • Tordis Ustad
    Affiliations
    Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway

    Department of Clinical Services, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway
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  • Marjaana Tikanmäki
    Affiliations
    PEDEGO Research Unit, MRC Oulu, Oulu University Hospital and University of Oulu, Oulu, Finland

    Finnish Institute for Health and Welfare, Public Health Promotion Unit, Helsinki, Oulu, Finland
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  • Peija Haaramo
    Affiliations
    Finnish Institute for Health and Welfare, Public Health Promotion Unit, Helsinki, Oulu, Finland
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  • Eero Kajantie
    Affiliations
    Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway

    PEDEGO Research Unit, MRC Oulu, Oulu University Hospital and University of Oulu, Oulu, Finland

    Finnish Institute for Health and Welfare, Public Health Promotion Unit, Helsinki, Oulu, Finland

    Children's Hospital, Helsinki University Hospital and University of Helsinki, Helsinki, Finland
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Open AccessPublished:May 19, 2020DOI:https://doi.org/10.1016/j.siny.2020.101116

      Abstract

      We reviewed literature on long-term motor outcomes of individuals aged five years or older born very preterm (VP: ≤32 weeks of gestation) or with very low birth weight (VLBW: ≤1500g), without cerebral palsy (CP). PubMed produced 2827 articles, whereof 38 were eligible. Assessed by standardised and norm-based motor tests, the Movement Assessment Battery for Children being the most widely used, VP/VLBW individuals showed poorer motor skills compared with term-born controls with differences of approximately 1 SD in magnitude. Some studies assessed subdomains and differences were present in fine motor/manual dexterity, ball skills and gross motor/balance. Prevalence of motor problems varied largely from 8-37% in studies with cut-off at the 5th percentile or −1.5 SD to 12–71% in studies with cut-off at the 15th percentile or −1 SD. This review shows that the degree of motor impairments continues to be substantial among VP/VLBW individuals who do not develop CP.

      Keywords

      1. Introduction

      Motor function is one of the very early signs of typical or adverse neurodevelopment in the child's first year of life [
      • Ferrari F.
      • et al.
      Preterm birth and developmental problems in the preschool age. Part I: minor motor problems.
      ]. Motor impairments that might be seen in children born preterm vary from cerebral palsy (CP) to minor or subtle motor problems. Most children do not develop CP [
      • Allen M.C.
      Neurodevelopmental outcomes of preterm infants.
      ], and minor motor problems might not be evident before early school age when being competent in various motor skills becomes increasingly important for everyday life activities [
      • Allen M.C.
      Neurodevelopmental outcomes of preterm infants.
      ]. Fine motor skills or manual dexterity are required for writing, typing, drawing and manipulating objects, while gross motor or balance skills are required amongst others for walking, running and jumping. Further, ball skills include both fine and gross motor skills, and are important for many sports and leisure activities as the child grows older.
      Motor problems have been consistently reported in children born very preterm (VP: ≤32 weeks) and/or with very low birth weight (VLBW: ≤1500 g). Over the past decades, there has been increased survival of VP/VLBW children, due to advances in prenatal and newborn care. However, rates of adverse neurodevelopmental outcomes have been relatively stable, with a slight decrease in moderate to severe CP [
      • Platt M.J.
      • et al.
      Trends in cerebral palsy among infants of very low birthweight (<1500 g) or born prematurely (<32 weeks) in 16 European centres: a database study.
      ,
      • McGowan E.C.
      • Vohr B.R.
      Neurodevelopmental follow-up of preterm infants: what is new?.
      ,
      • Fawke J.
      Neurological outcomes following preterm birth.
      ] and an increase in non-CP motor impairment among extremely preterm (EP: ≤28 weeks) and/or extremely low birth weight (ELBW: ≤1000g) [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ,
      • Cheong J.L.Y.
      Have outcomes following extremely preterm birth improved over time?.
      ].
      Motor problems, or developmental coordination disorder (DCD) as used by some authors, are usually defined as a score below a cut-off on a standardised motor test, compared with a normative sample or a control group. There are different recommendations as to cut-offs, ranging from scores −2 SD or <5th percentile [
      • Henderson S.E.
      • Sugden D.A.
      • Barnett A.L.
      Movement Assessment Battery for Children-2. Examiner's manual.
      ] to −1 SD or < 15th percentile [
      • Blank R.
      • et al.
      International clinical practice recommendations on the definition, diagnosis, assessment, intervention, and psychosocial aspects of developmental coordination disorder.
      ].
      Three systematic reviews on motor outcomes of VP/VLBW survivors have been published previously [
      • Edwards J.
      • et al.
      Developmental coordination disorder in school-aged children born very preterm and/or at very low birth weight: a systematic review.
      ,
      • de Kieviet J.F.
      • Piek J.P.
      • Aarnoudse-Moens C.S.
      • Oosterlaan J.
      Motor development in very preterm and very low-birth-weight children from birth to adolescence: a meta-analysis.
      ,
      • FitzGerald T.L.
      • Kwong A.K.L.
      • Cheong J.L.Y.
      • McGinley J.L.
      • Doyle L.W.
      • Spittle A.J.
      Body structure, function, activity, and participation in 3- to 6-year-old children born very preterm: an ICF-based systematic review and meta-analysis.
      ], and in addition, five reviews including any children born preterm or with low birth weight (<37 weeks/<2500 g) [
      • Allotey J.
      • et al.
      Cognitive, motor, behavioural and academic performances of children born preterm: a meta-analysis and systematic review involving 64 061 children.
      ,
      • Williams J.
      • Lee K.J.
      • Anderson P.J.
      Prevalence of motor-skill impairment in preterm children who do not develop cerebral palsy: a systematic review.
      ,
      • Moreira R.S.
      • Magalhães L.C.
      • Alves C.R.L.
      Effect of preterm birth on motor development, behavior, and school performance of school-age children: a systematic review.
      ,
      • Upadhyay R.P.
      • et al.
      Cognitive and motor outcomes in children born low birth weight: a systematic review and meta-analysis of studies from South Asia.
      ,
      • Bos A.F.
      • Van Braeckel K.N.J.A.
      • Hitzert M.M.
      • Tanis J.C.
      • Roze E.
      Development of fine motor skills in preterm infants.
      ]. De Kieviet et al., 2009 [
      • de Kieviet J.F.
      • Piek J.P.
      • Aarnoudse-Moens C.S.
      • Oosterlaan J.
      Motor development in very preterm and very low-birth-weight children from birth to adolescence: a meta-analysis.
      ] investigated the relationship between VP/VLBW and motor development from birth through adolescence. In comparison with term-born peers, VP/VLBW children obtained significantly lower scores on all the three motor tests included: the Bayley Scales of Infant Development version II, the Movement Assessment Battery for Children (Movement ABC) and the Bruininks-Oseretsky Test of Motor Proficiency (BOTMP). Edwards et al., 2011 [
      • Edwards J.
      • et al.
      Developmental coordination disorder in school-aged children born very preterm and/or at very low birth weight: a systematic review.
      ] concluded that DCD was more prevalent in the VP/VLBW population than full-term/normal birth weight children, with significantly greater odds of developing the disorder (6.29; 95%CI: 4.37–9.05 for scoring <5th percentile and 8.66; 95%CI: 3.40–22.07 for scoring 5 to 15th percentile). Both reviews included several studies that did not exclude children with mild CP. FitzGerald et al., 2018 [
      • FitzGerald T.L.
      • Kwong A.K.L.
      • Cheong J.L.Y.
      • McGinley J.L.
      • Doyle L.W.
      • Spittle A.J.
      Body structure, function, activity, and participation in 3- to 6-year-old children born very preterm: an ICF-based systematic review and meta-analysis.
      ] concluded that VP children aged 3–6 years had poorer motor outcomes compared with term-born children using the International Classification of Functioning, Disability and Health domains of body structure and function and activity.
      We aimed to review long-term motor outcomes including domain-specific motor skills, assessed by standardised motor tests, of VP/VLBW children with no manifest CP compared with term-born controls. We also examined the prevalence of motor problems in VP/VLBW children and risk factors for these problems. We focused on individuals ≥5 years of age, which is a commonly used cut-off in health statistics and the age when hospital follow-up programmes generally are terminated.

      2. Methods

      A comprehensive literature search was carried out by one author (PH) in MEDLINE Database, using PubMed, between 8 October and 6 November 2019. The search produced 2827 articles (Fig. 1). Search terms are listed in Appendix A.
      Fig. 1
      Fig. 1Flow of article selection for review. CP: Cerebral palsy; VLBW: Very low birth weight; VP: Very preterm.
      One author (KAIE) conducted the initial screening of titles and abstracts, using the following inclusion criteria: exposure was VP/VLBW (gestational age ≤32 weeks or birth weight ≤1500g), age of assessment ≥5 years, motor outcome was assessed by a standardised and norm-based motor test, the results were reported as continuous scores (mean/median) compared with a control group or as proportion of children with motor problems according to a defined cut-off. The studies had to be observational cohort studies, exclude participants with all degrees of CP or present results for participants without CP. No study population size or publication year restrictions were applied. Included studies had to be original research articles with full-text available in English. If more than one study reported the same findings on the same cohort assessed at the same age only the publication on the original or larger study sample was included in the review.
      Two authors (KAIE and TU) assessed the 230 remaining articles for eligibility, checking the full-texts against the above criteria, resulting in 38 original articles for the final review (Fig. 1). Key characteristics and outcomes were extracted and entered into Table 1, Table 2 by four authors (KAIE, TU, MT and PH). A qualitative synthesis of the included studies was performed.
      Table 1Characteristics of included articles in the order of years of birth of the study participants.
      CitationSettingDesign (n)BW/GA criteriaExclusionsTerm control groupBirth yearMean ageMotor outcomeContinuous motor test scores
      Compared with term-born controls.
      Cut-off for motor problemsRisk factors
      Modifiers of the association between VP/VLBW and motor outcome, such as other perinatal risk factors, parental factors or sex differences.
      Klein et al., 1989 [
      • Klein N.K.
      • Hack M.
      • Breslau N.
      Children who were very low birth weight: development and academic achievement at nine years of age.
      ]
      USAHospital-based cohort (n = 65)≤1500gCP, congenital cataracts, fetal alcohol syndrome, mental retardationYes19769.3 yPurdue PegboardMean (SD)NoYes
      Saigal et al., 1991 [
      • Saigal S.
      • Rosenbaum P.
      • Szatmari P.
      • Campbell D.
      Learning disabilities and school problems in a regional cohort of extremely low birth weight (less than 1000 G) children: a comparison with term controls.
      ]
      CanadaRegional cohort (n = 68)<1000gCP, hydrocephalus, IQ < 85, blindness, deafnessYes1977–19817.8 yBOTMPMean (SD)NoNo
      Marlow et al., 1989 [
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ]
      EnglandHospital-based cohort (n = 53)<1251gCPYes1980–19816.1 yTOMIMedian (IQR)NoYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Marlow et al., 1993 [
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ]
      EnglandHospital-based cohort (n = 51)<1251gCPYes1980–19818.0 yTOMIMedian (IQR)NoNo
      Powls et al., 1995 [
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ]
      EnglandHospital-based cohort (n = 47)<1251gMajor neuro-developmental impairment (no CP reported by Marlow et al. [
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ,
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ])
      Yes1980–198112-13 yMovement ABCMedian (IQR)<5th percentile; <15th percentileYes
      Holsti et al., 2002 [
      • Holsti L.
      • Grunau R.V.E.
      • Whitfield M.F.
      Developmental coordination disorder in extremely low birth weight children at nine years.
      ]
      CanadaRegional cohort (n = 73)≤800gNeurosensory handicaps, ambulatory CP, verbal and performance IQ < 85Yes1982–19878.8 yBOTMPNo
      Continuous motor scores not reported for the total ELBW group.
      <-2SD
      <-2SD not shown in Fig. 2.
      ;

      <-1.5SD;

      <-1SD
      Yes
      Weindrich et al., 2003 [
      • Weindrich D.
      • Jennen-Steinmetz C.
      • Laucht M.
      • Schmidt M.H.
      Late sequelae of low birthweight: mediators of poor school performance at 11 years.
      ]
      GermanyRegional cohort (n = 29)<1500gCP, severe learning disability, blindnessYes1986–198810.9 yKTKMean (SE)
      Adjusted for sex and psychosocial risk.
      NoNo
      Evensen et al., 2009 [
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ]
      NorwayRegional cohort (n = 51)≤1500gCP, congenital anomalies, syndromesYes1986–198814.2 yMovement ABCMedian (IQR)<5th percentile; <15th percentileNo
      Husby et al., 2013 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ]
      NorwayRegional cohort, subsample (n = 36)≤1500gCongenital anomalies, syndromes. Results presented for adults without CP (n = 32)Yes1986–198822.5 yMovement ABC-2; HiMAT; GPMean (SD)No
      Proportion of motor problems not reported for VLBW adults without CP.
      No
      Wocadlo & Rieger 2008 [
      • Wocadlo C.
      • Rieger I.
      Motor impairment and low achievement in very preterm children at eight years of age.
      ]
      AustraliaHospital-based cohort (n = 323)<30 wksCP, IQ < 76, blindness, hearing impairmentNo1987–19978 yBOTMPNo≤5th percentile; <15th percentileYes
      Keller et al., 1998 [
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ]
      CanadaRegional cohort, subsample (n = 34)<1500g; <1000gNeuromuscular disabilityYes1988–19906.4 yKTKMean (SD)NoNo
      Short el al. 2003 [
      • Short E.J.
      • et al.
      Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.
      ]
      USARegional cohort (n = 173)<1500gResults presented for children without neurological problems (n = 104)Yes1989–19918 yBOTMP Short FormMean (SD)NoYes
      Davis et al., 2007 [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ]
      AustraliaRegional cohort (n = 255)<1000g/<28 wksCP, IQ < −2SDYes1991–19928.7 yMovement ABCMedian (IQR)<5th percentile; <15th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Torrioli et al., 2000 [
      • Torrioli M.G.
      • et al.
      Perceptual-motor, visual and cognitive ability in very low birthweight preschool children without neonatal ultrasound abnormalities.
      ]
      ItalyHospital-based cohort (n = 36)<1500gCP, mental retardation, blindness, deafness, born with specific diseasesYes1991–19934.9 yMovement ABCMean (SD)≤15th percentileYes
      Rademaker et al., 2004 [
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ]
      The NetherlandsRegional cohort (n = 204)≤1500g/≤32 wksCongenital abnormalities, chromosomal disorders. Results presented for children without CP (n = 189)Yes1991–19937-8yMovement ABCMedian (range)<5th percentile; ≤15th percentileNo
      Seitz et al., 2006 [
      • Seitz J.
      • Jenni O.G.
      • Molinari L.
      • Caflisch J.
      • Largo R.H.
      • Latal Hajnal B.
      Correlations between motor performance and cognitive functions in children born < 1250 g at school age.
      ]
      SwitzerlandHospital-based
      Tertiary centre.
      cohort (n = 74)
      <1250gCP, IQ < 70No1992–19946.0 yZNANo<10th percentileNo
      Natalucci et al., 2013 [
      • Natalucci G.
      • et al.
      Development of neuromotor functions in very low birth weight children from six to 10 years of age: patterns of change.
      ]
      SwitzerlandHospital-based
      Tertiary centre.
      cohort (n = 65)
      <1250gCP, mental retardation, severe behavioural problemsNo1992–199410.3 yZNANo<10th percentileNo
      Feder et al., 2005 [
      • Feder K.P.
      • Majnemer A.
      • Bourbonnais D.
      • Platt R.
      • Blayney M.
      • Synnes A.
      Handwriting performance in preterm children compared with term peers at age 6 to 7 years.
      ]
      CanadaRegional cohort (n = 42)<1250g/<34 wksCP, cognitive impairment, chromosomal abnormalities, genetic syndromes, visual or hearing impairment, IVH grade 3Yes1992–19946.6 yBOTMP subtestsMean (SD)NoNo
      Zanudin et al., 2012 [
      • Zanudin A.
      • Gray P.H.
      • Burns Y.
      • Danks M.
      • Watter P.
      • Poulsen L.
      Perinatal factors in non-disabled ELBW school children and later performance.
      ]
      AustraliaHospital-based cohort (n = 48)<1000gCP, general cognitive ability <-2SD at 4 yNo1992–199412.4 yMovement ABCNo≤15th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Hack et al., 2005 [
      • Hack M.
      • et al.
      Chronic conditions, functional limitations, and special health care needs of school-aged children born with extremely low-birth-weight in the 1990s.
      ]
      USAHospital-based
      Tertiary centre.
      cohort (n = 219)
      <1000gResults presented for children without CP, deafness or blindness (n = 183)Yes1992–19958 yBOTMP Short FormNo<-2SD; <-1SDNo
      Goyen & Lui 2009 [
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ]
      AustraliaHospital-based
      Tertiary centre.
      cohort (n = 50)
      <1000g/<29 wksCP, IQ < 85, visual or hearing impairmentYes1992–19958.8 yMovement ABCMedian (IQR)<-1.5SD (5th percentile); <-1SD (15th percentile)Yes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Esbjørn et al., 2006 [
      • Esbjørn B.H.
      • Hansen B.M.
      • Greisen G.
      • Mortensen E.L.
      Intellectual development in a Danish cohort of prematurely born preschool children: specific or general difficulties?.
      ]
      DenmarkNational cohort (n = 207)<1000g/<28 wksResults presented for children without CP or visual impairments (n = 190)Yes1994–19955.1 yMovement ABCMean (SD); adjusted mean (SEM)
      Adjusted for age and parental education.
      NoNo
      Marlow et al., 2007 [
      • Marlow N.
      • Hennessy E.M.
      • Bracewell M.A.
      • Wolke D.
      EPICure Study Group
      Motor and executive function at 6 years of age after extremely preterm birth.
      ]
      UK and IrelandNational cohort (n = 180)≤25 wksCP or hypotonia resulting in reduced mobilityYes19956.3 yMovement ABC subtestsMedian (IQR)NoYes
      Dewey et al., 2011 [
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ]
      CanadaRegional cohort (n = 103)≤1000gCP, IQ < 70, visual impairmentNoNot reported (assessed 2001–2005)5 yMovement ABCNo≤15th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Janssen et al., 2009 [
      • Janssen A.J.W.M.
      • Nijhuis-van der Sanden M.W.G.
      • Akkermans R.P.
      • Tissingh J.
      • Oostendorp R.A.B.
      • Kollée L.A.A.
      A model to predict motor performance in preterm infants at 5 years.
      ]
      The NetherlandsHospital-based cohort (n = 371)≤32 wksCP, chromosomal disorders, neuromuscular diseasesNo1996–20015.3 yMovement ABCNo<15th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Spittle et al., 2018 [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ]
      AustraliaRegional cohort (n = 189; 191)<1000g/<28 wksResults presented for children without CP (n = 168; 169)Yes1997; 20058 yMovement ABC; MovementABC-2No<5th percentile; ≤5th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Leversen et al., 2011 [
      • Leversen K.T.
      • et al.
      Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm.
      ]
      NorwayNational cohort (n = 306)<1000g/<28 wksResults presented for children without CP, blindness, deafness or autism (n = 261)No1999–20005.8 yMovement ABCNo<5th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Grunewaldt et al., 2014 [
      • Grunewaldt K.H.
      • et al.
      Follow-up at age 10 years in ELBW children - functional outcome, brain morphology and results from motor assessments in infancy.
      ]
      NorwayRegional cohort (n = 31)<1000gCongenital syndromes. Results presented for children without CP (n = 23)Yes1999–200110.2 yMovementABC-2Mean (95% CI)NoNo
      Tanis et al., 2012 [
      • Tanis J.C.
      • et al.
      Functional outcome of very preterm-born and small-for-gestational-age children at school age.
      ]
      The NetherlandsHospital-based cohort (n = 56)<32 wks, SGA and AGAChromosomal and congenital abnormalities, none had CPNo (VP AGA as control)2000–20018.6 yMovement ABCNo<5th percentile; ≤15th percentileYes
      Flamand et al., 2012 [
      • Flamand V.H.
      • Nadeau L.
      • Schneider C.
      Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm.
      ]
      CanadaHospital-based cohort, subsample (n = 10)≤32 wksCP, stroke, sensory impairment, small size for GA, IQ < 70, medication for ADHD, twins, neonatal complicationsYesNot reported8.5 yMovement ABCMean (SD) percentile≤5th percentile; ≤15th percentileYes
      Zwicker et al., 2013 [
      • Zwicker J.G.
      • Yoon S.W.
      • Mackay M.
      • Petrie-Thomas J.
      • Rogers M.
      • Synnes A.R.
      Perinatal and neonatal predictors of developmental coordination disorder in very low birthweight children.
      ]
      CanadaHospital-based cohort (n = 157)<1250gCP, IQ < 70, blindnessNoNot reported (assessed 2005–2009)4.5 y-5.9 yMovement ABCNo≤5th percentile; ≤15th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Oliveira et al., 2011 [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ]
      BrazilRegional cohort (n = 23)≤1500gNeurological and orthopedic problems, malformations, syndromes, sensory deficits or other disabilitiesYes2001–20025.8 yMovement ABCMean (SD)<5th percentile; <15th percentileYes
      Spittle et al., 2011 [
      • Spittle A.J.
      • et al.
      Neonatal white matter abnormality predicts childhood motor impairment in very preterm children.
      ]
      AustraliaHospital-based cohort (n = 193)<1250g/<30 wksGenetic or congenital abnormalities. Results presented for children without CP (n = 178)No2001–20035 yMovement ABCNo≤5th percentile; ≤15th percentileYes
      Setänen et al., 2016 [
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ]
      FinlandRegional cohort (n = 98)≤1500g/<32 wksResults presented for children without CP (n = 90)No2001–200411.2 yMovementABC-2No≤5th percentile; ≤15th percentileYes
      Kurpershoek et al., 2016 [
      • Kurpershoek T.
      • Potharst-Sirag E.S.
      • Aarnoudse-Moens C.S.H.
      • van Wassenaer-Leemhuis A.G.
      Minor neurological dysfunction in five year old very preterm children is associated with lower processing speed.
      ]
      The NetherlandsHospital-based cohort (n = 94)<1000g/<30 wksSevere handicaps, genetic syndrome. Results presented for children without CP (n = 76)NoNot reported (assessed 2007–2009)5 yMovementABC/ABC-2No≤5th percentile; ≤15th percentileNo
      Moreira et al., 2014 [
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ]
      BrazilHospital-based cohort (n = 100)<1500g/<35 wksAbnormal neurological conditionsNo2002–20049.4 yMovementABC-2No<15th percentileYes
      Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      Janssen et al., 2016 [
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ]
      The NetherlandsHospital-based cohort (n = 201)<32 wksCP, blindness, deafness, syndromesNo2003–20055.3 yMovementABC-2No<-2SD
      <-2SD not shown in Fig. 2.
      ; <-1SD
      Yes
      Bolk et al., 2018 [
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ]
      SwedenNational cohort (n = 229)<27 wksCP, cognitive impairment <-2SD, visual or hearing impairmentYes2004–20076.5 yMovementABC-2No≤5th percentile
      Odds ratio adjusted for mother's education, mother's country of birth, complex sample analysis to adjust for clustering effects caused by presence of twins.
      ≤15th percentile
      Yes
      ADHD: Attention Deficit Hyperactivity Disorder; AGA: Appropriate for gestational age; BOTMP: Bruininks-Oseretsky Test of Motor Proficiency; BW: Birth weight; CI: Confidence interval; CP: Cerebral palsy; ELBW: Extremely low birth weight; GA: Gestational age; GP: Grooved Pegboard; HiMAT: High-Level Mobility Assessment Tool; IVH: Intraventricular haemorrhage; IQ: Intellectual quotient; IQR: Interquartile range; KTK: Körperkoordinationstest für Kinder; Movement ABC: Movement Assessment Battery for Children; Movement ABC-2: Movement Assessment Battery for Children-Second edition; SD: Standard deviation; SE: Standard error; SEM: Standard error of measurement; SGA: Small for gestational age; TOMI: Test of Motor Impairment; VP: Very preterm; VLBW: Very low birth weight, ZNA: Zurich Neuromotor Assessment.
      a Compared with term-born controls.
      b Modifiers of the association between VP/VLBW and motor outcome, such as other perinatal risk factors, parental factors or sex differences.
      c Multivariate or multiple regression analyses (only significant variables in the final model reported in this manuscript).
      d Continuous motor scores not reported for the total ELBW group.
      e <-2SD not shown in Fig. 2.
      f Adjusted for sex and psychosocial risk.
      g Proportion of motor problems not reported for VLBW adults without CP.
      h Tertiary centre.
      i Adjusted for age and parental education.
      j Odds ratio adjusted for mother's education, mother's country of birth, complex sample analysis to adjust for clustering effects caused by presence of twins.
      Table 2Total motor test scores of VP/VLBW individuals without CP compared with controls as reported in the included articles.
      CitationVP/VLBW n (% male)Control n (% male)VP/VLBWControlp-valueDifference in mean/medianDifference in SD units
      Based on SD of control group.
      Movement ABC
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD/SEM)
      Torrioli et al., 2000 [
      • Torrioli M.G.
      • et al.
      Perceptual-motor, visual and cognitive ability in very low birthweight preschool children without neonatal ultrasound abnormalities.
      ]
      n = 36 (42%)Not reported (matched)15.58 (7.96)7.08 (4.61)p < 0.0018.51.84
      Esbjørn et al., 2006 [
      • Esbjørn B.H.
      • Hansen B.M.
      • Greisen G.
      • Mortensen E.L.
      Intellectual development in a Danish cohort of prematurely born preschool children: specific or general difficulties?.
      ]
      n = 190 (49% of original sample, n = 269)n = 76 (46%)10.5 (7.8)

      10.7 (SEM 0.6)
      Adjusted for age and parental education.
      6.5 (4.3)

      5.5 (SEM 1.1)
      Adjusted for age and parental education.
      p < 0.001

      p < 0.001
      4.0

      5.2
      0.93

      1.21
      Flamand et al., 2012 [
      • Flamand V.H.
      • Nadeau L.
      • Schneider C.
      Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm.
      ]
      n = 10 (60%)n = 7 (57%)32.7th (26.5) percentile60.6th (19.8) percentilep = 0.03827.91.41
      Oliveira et al., 2011 [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ]
      n = 23 (39%)n = 23 (not reported)8.17 (7.10)3.06 (3.80)p = 0.0025.11.34
      Movement ABC-2
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD/95% CI)
      Husby et al., 2013 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ]
      n = 32 (38%)n = 37 (41%)74.1 (14.4)80.2 (8.7)p = 0.0616.10.70
      Grunewaldt et al., 2014 [
      • Grunewaldt K.H.
      • et al.
      Follow-up at age 10 years in ELBW children - functional outcome, brain morphology and results from motor assessments in infancy.
      ]
      n = 23 (35%)n = 33(49%)63.8 (55.8–71.8)77.1 (70.6–83.6)p = 0.01913.3
      TOMI/Movement ABC/Movement ABC-2
      Scoring is shown in Appendix B. Table 1.
      ; median (IQR)
      Marlow et al., 1989 [
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ]
      n = 53 (62%)n = 53 (62%)6.0 (4.0–8.75)3.0 (1.5–4.5)p < 0.0013.0
      Marlow et al., 1993 [
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ]
      n = 51 (63%)n = 59 (not reported)3.5 (3–5)2.0 (1–4)p = 0.00021.5
      Powls et al., 1995 [
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ]
      n = 47 (not reported)n = 60 (not reported)10 (3.5–16)2.5 (0.5–6)p < 0.00017.5
      Evensen et al., 2009 [
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ]
      n = 51 (55%)n = 75 (43%)10.0 (5.0–14.0)6.5 (3.0–9.0)p < 0.0013.5
      Davis et al., 2007 [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ]
      n = 255 (46%)n = 208 (not reported)4.5 (2.0–10.5)1.5 (0.5–3.5)p < 0.0013.0
      Rademaker et al., 2004 [
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ]
      n = 189 (57%)n = 21 (62%)5.5 (range 0–36.5)2.0 (range 0–10)Not reported3.5
      Goyen & Lui 2009 [
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ]
      n = 50 (50%)Not reported (matched)8.75 (5–13.6)5 (2.9–9.7)p < 0.0013.75
      BOTMP
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD)
      Saigal et al., 1991 [
      • Saigal S.
      • Rosenbaum P.
      • Szatmari P.
      • Campbell D.
      Learning disabilities and school problems in a regional cohort of extremely low birth weight (less than 1000 G) children: a comparison with term controls.
      ]
      n = 68 (44%)n = 114 (47%)46.6 (8.9)54.6 (9.4)p < 0.00018.00.85
      Short el al. 2003 [
      • Short E.J.
      • et al.
      Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.
      ]
      BPD n = 49 (45%)

      VLBW n = 55 (40%)
      n = 99 (49%)BPD 47.1 (13)

      VLBW 52.9 (12)
      57.8 (12)p = 0.001 for both groups vs. Control10.7

      4.9
      0.89

      0.41
      KTK
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD)
      Weindrich et al., 2003 [
      • Weindrich D.
      • Jennen-Steinmetz C.
      • Laucht M.
      • Schmidt M.H.
      Late sequelae of low birthweight: mediators of poor school performance at 11 years.
      ]
      n = 29 (38%)n = 112 (49%)98.4 (SE 2.6)
      Adjusted for sex and psychosocial risk.
      105.4 (SE 1.3)
      Adjusted for sex and psychosocial risk.
      p < 0.057.0
      Keller et al., 1998 [
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ]
      ELBW n = 14 (21%)

      VLBW n = 20 (75%)
      n = 24 (63%)ELBW 73 (10)

      VLBW 82 (11)
      85 (8)p < 0.05 for ELBW vs. VLBW and Control12.0

      3.0
      1.50

      0.38
      HiMAT
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD)
      Husby et al., 2013 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ]
      n = 32 (38%)n = 37 (41%)46.6 (5.4)49.6 (3.4)p = 0.0233.00.88
      GP
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD)
      Husby et al., 2013 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ]
      n = 32 (38%)n = 37 (41%)Dominant hand68.5 (16.9)62.2 (9.5)p = 0.0646.30.66
      Non-dominant hand73.9 (13.4)68.3 (10.6)p = 0.0615.60.53
      Purdue Pegboard
      Scoring is shown in Appendix B. Table 1.
      ; mean (SD)
      Klein et al., 1989 [
      • Klein N.K.
      • Hack M.
      • Breslau N.
      Children who were very low birth weight: development and academic achievement at nine years of age.
      ]
      n = 65 (62%)n = 65 (62%)Combined hands8 (2)9 (2)p < 0.0071.00.50
      Right hand11 (2)12 (2)<0.051.00.50
      Left hand10 (2)11 (2)<0.0251.00.50
      BOTMP: Bruininks-Oseretsky Test of Motor Proficiency; BPD: Bronchopulmonal dysplasia; CI: Confidence interval; CP: Cerebral palsy; ELBW: Extremely low birth weight; GP: Grooved Pegboard; HiMAT: High-Level Mobility Assessment Tool; IQR: Interquartile range; KTK: Körperkoordinationstest für Kinder; Movement ABC: Movement Assessment Battery for Children; Movement ABC-2: Movement Assessment Battery for Children-Second edition; SD: Standard deviation; SE: Standard error; SEM: Standard error of measurement; TOMI: Test of Motor Impairment; VP: Very preterm; VLBW: Very low birth weight.
      a Based on SD of control group.
      b Scoring is shown in Appendix B. Table 1.
      c Adjusted for age and parental education.
      d Adjusted for sex and psychosocial risk.

      3. Results

      3.1 Characteristics of included articles

      Table 1 shows characteristics of the included articles, published between 1989 and 2018. Birth year of participants ranged from 1976 to 2007 and mean age at assessment was 5–22.5 years. Twenty-four articles reported outcomes for VP/VLBW and 14 for EP/ELBW children. Included articles were from high-income countries in Europe (n = 20), Australia (n = 6), Canada (n = 7), USA (n = 3) and a middle-income country (Brazil; n = 2) and used the following motor tests: the Movement ABC [
      • Henderson S.E.
      • Sugden D.A.
      Movement Assessment Battery for Children. Manual.
      ] (n = 18), the Movement Assessment Battery for Children-Second edition [
      • Henderson S.E.
      • Sugden D.A.
      • Barnett A.L.
      Movement Assessment Battery for Children-2. Examiner's manual.
      ] (Movement ABC-2) (n = 7), the BOTMP [
      • Bruininks R.H.
      Bruininks-Oseretsky Test of Motor Proficiency: examiner's manual. Circle pines.
      ] (n = 6), the Test of Motor Impairment (TOMI) [
      • Stott D.
      • Moyes F.
      • Henderson S.
      Test of Motor Impairment.
      ] (n = 2) (the precursor of Movement ABC), the Körperkoordinationstest für Kinder (KTK) [
      • Weindrich D.
      • Jennen-Steinmetz C.
      • Laucht M.
      • Schmidt M.H.
      Late sequelae of low birthweight: mediators of poor school performance at 11 years.
      ,
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ] (n = 2), the Zurich Neuromotor Assessment (ZNA) [
      • Largo R.H.
      • et al.
      Neuromotor development from 5 to 18 years. Part 1: timed performance.
      ,
      • Largo R.H.
      • Caflisch J.A.
      • Hug F.
      • Muggli K.
      • Molnar A.A.
      • Molinari L.
      Neuromotor development from 5 to 18 years. Part 2: associated movements.
      ] (n = 2), the High-Level Mobility Assessment Tool (HiMAT) [
      • Williams G.
      • Morris M.
      • Greenwood K.
      • Goldie P.
      • Robertson V.
      High-level Mobility Assessment Tool for traumatic brain injury. HiMAT user manual. Melbourne: school of physiotherapy.
      ] (n = 1), the Grooved Pegboard (n = 1) [
      ] or the Purdue Pegboard [
      ] (n = 1) (Appendix B. Table 1).

      3.2 Total motor test scores of VP/VLBW individuals without CP compared with term-born controls

      Eighteen articles reported continuous total test scores compared with a term-born control group (Table 2). In studies with more than 20 participants, the VP/VLBW children had mean Movement ABC scores 4.0 to 8.5 points lower compared with controls at 5–6 years of age [
      • Esbjørn B.H.
      • Hansen B.M.
      • Greisen G.
      • Mortensen E.L.
      Intellectual development in a Danish cohort of prematurely born preschool children: specific or general difficulties?.
      ,
      • Torrioli M.G.
      • et al.
      Perceptual-motor, visual and cognitive ability in very low birthweight preschool children without neonatal ultrasound abnormalities.
      ,
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ], corresponding to differences ranging from 0.93 [
      • Esbjørn B.H.
      • Hansen B.M.
      • Greisen G.
      • Mortensen E.L.
      Intellectual development in a Danish cohort of prematurely born preschool children: specific or general difficulties?.
      ] to 1.84 SD [
      • Torrioli M.G.
      • et al.
      Perceptual-motor, visual and cognitive ability in very low birthweight preschool children without neonatal ultrasound abnormalities.
      ]. Mean Movement ABC-2 scores were 6.1 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] to 13.3 [
      • Grunewaldt K.H.
      • et al.
      Follow-up at age 10 years in ELBW children - functional outcome, brain morphology and results from motor assessments in infancy.
      ] points lower, corresponding to a 0.70 SD difference in young adults [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ]. The difference in median TOMI, Movement ABC or Movement ABC-2 scores ranged from 1.5 to 7.5 points in children aged 6–14 years [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ,
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ,
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ,
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ]. Assessed by the BOTMP, mean differences were 10.7 and 4.9 points in VLBW children with and without BPD [
      • Short E.J.
      • et al.
      Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.
      ], and 8.0 points in ELBW children [
      • Saigal S.
      • Rosenbaum P.
      • Szatmari P.
      • Campbell D.
      Learning disabilities and school problems in a regional cohort of extremely low birth weight (less than 1000 G) children: a comparison with term controls.
      ], corresponding to 0.41 to 0.89 SD difference from their respective control groups at 8 years of age. Measured by the KTK, differences in mean scores between VLBW and control groups ranged from 3 [
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ] to 7 points [
      • Weindrich D.
      • Jennen-Steinmetz C.
      • Laucht M.
      • Schmidt M.H.
      Late sequelae of low birthweight: mediators of poor school performance at 11 years.
      ] and was as large as 12 points (1.50 SD) in ELBW children compared with controls at 6 years [
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ]. The only adult study [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] reported a difference of 3 points (0.88 SD) between the VLBW and the control group at 22.5 years of age, assessed by the HiMAT. VLBW adults used 5.6–6.3 s more than controls to complete the GP with the non-dominant and dominant hand, a difference of 0.53 and 0.66 SD, respectively [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ], similar to the 0.50 SD difference in performance on the Purdue Pegboard in 9-year-old children for all three conditions [
      • Klein N.K.
      • Hack M.
      • Breslau N.
      Children who were very low birth weight: development and academic achievement at nine years of age.
      ] (Table 2).

      3.3 Domain-specific test scores of VP/VLBW individuals without CP compared with term-born controls

      Eleven articles reported continuous test scores for subdomains of manual dexterity/fine motor function, ball skills and balance/gross motor function (data not shown). Mean manual dexterity scores on Movement ABC were 1.9 points lower [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ], and on Movement ABC-2 2.1 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] to 7.7 [
      • Grunewaldt K.H.
      • et al.
      Follow-up at age 10 years in ELBW children - functional outcome, brain morphology and results from motor assessments in infancy.
      ] points lower, in VP/VLBW individuals compared with controls, corresponding to differences of 0.39 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] to 0.91 SD [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ]. Differences in median TOMI or Movement ABC manual dexterity scores ranged from 0.5 to 2.0 points [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ,
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ], and was 1.5 points lower for posting coins in ELBW children [
      • Marlow N.
      • Hennessy E.M.
      • Bracewell M.A.
      • Wolke D.
      EPICure Study Group
      Motor and executive function at 6 years of age after extremely preterm birth.
      ]. VLBW children had BOTMP scores 1.3 to 5.2 points lower for fine motor and upper limb tasks, and differences ranged from 0.34 to 0.63 SD for the various subtests [
      • Feder K.P.
      • Majnemer A.
      • Bourbonnais D.
      • Platt R.
      • Blayney M.
      • Synnes A.
      Handwriting performance in preterm children compared with term peers at age 6 to 7 years.
      ].
      For ball skills, VP/VLBW individuals had Movement ABC scores 1.5 points lower [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ], and Movement ABC-2 scores 1.1 [
      • Grunewaldt K.H.
      • et al.
      Follow-up at age 10 years in ELBW children - functional outcome, brain morphology and results from motor assessments in infancy.
      ] to 1.4 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] points lower compared with controls, corresponding to differences of 0.30 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] to 1.66 SD [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ]. The difference in median TOMI and Movement ABC ball skills scores ranged from 0.5 to 1.0 points [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ,
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ].
      In the balance domain, VP/VLBW individuals had Movement ABC-2 scores 2.5 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] to 5.1 points [
      • Grunewaldt K.H.
      • et al.
      Follow-up at age 10 years in ELBW children - functional outcome, brain morphology and results from motor assessments in infancy.
      ] lower and Movement ABC scores 1.8 points [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ] lower than controls, corresponding to a 0.64 [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ] to 0.96 SD difference [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ]. Differences in median Movement ABC and TOMI balance scores ranged from 0.5 to 2.0 points [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Marlow N.
      • Roberts L.
      • Cooke R.
      Outcome at 8 years for children with birth weights of 1250 g or less.
      ,
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ], and were 1.0–2.0 points for heel-toe walking and one-leg balance, respectively [
      • Marlow N.
      • Hennessy E.M.
      • Bracewell M.A.
      • Wolke D.
      EPICure Study Group
      Motor and executive function at 6 years of age after extremely preterm birth.
      ]. Differences in balance, laterality and jumping task scores of the KTK ranged from 0.50 to 1.00 SD for ELBW children and from 0.13 to 0.62 SD for VLBW children versus controls [
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ].

      3.4 Prevalence of motor problems in VP/VLBW individuals without CP

      Prevalence of motor problems among VP/VLBW individuals assessed by the Movement ABC or Movement ABC-2 varied from 7.9 to 37.1% in studies with cut-off at the 5th percentile or −1.5 SD [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ,
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ,
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ,
      • Leversen K.T.
      • et al.
      Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm.
      ,
      • Tanis J.C.
      • et al.
      Functional outcome of very preterm-born and small-for-gestational-age children at school age.
      ,
      • Flamand V.H.
      • Nadeau L.
      • Schneider C.
      Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm.
      ,
      • Zwicker J.G.
      • Yoon S.W.
      • Mackay M.
      • Petrie-Thomas J.
      • Rogers M.
      • Synnes A.R.
      Perinatal and neonatal predictors of developmental coordination disorder in very low birthweight children.
      ,
      • Spittle A.J.
      • et al.
      Neonatal white matter abnormality predicts childhood motor impairment in very preterm children.
      ,
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ,
      • Kurpershoek T.
      • Potharst-Sirag E.S.
      • Aarnoudse-Moens C.S.H.
      • van Wassenaer-Leemhuis A.G.
      Minor neurological dysfunction in five year old very preterm children is associated with lower processing speed.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ], with one third of the studies reporting motor problems in more than a quarter of the children aged 6 to 12–13 years of age (Fig. 2). In studies with cut-off at the 15th percentile or −1 SD, the prevalence ranged from 12.2 to 70.6% [
      • Torrioli M.G.
      • et al.
      Perceptual-motor, visual and cognitive ability in very low birthweight preschool children without neonatal ultrasound abnormalities.
      ,
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ,
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ,
      • Tanis J.C.
      • et al.
      Functional outcome of very preterm-born and small-for-gestational-age children at school age.
      ,
      • Flamand V.H.
      • Nadeau L.
      • Schneider C.
      Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm.
      ,
      • Zwicker J.G.
      • Yoon S.W.
      • Mackay M.
      • Petrie-Thomas J.
      • Rogers M.
      • Synnes A.R.
      Perinatal and neonatal predictors of developmental coordination disorder in very low birthweight children.
      ,
      • Spittle A.J.
      • et al.
      Neonatal white matter abnormality predicts childhood motor impairment in very preterm children.
      ,
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ,
      • Kurpershoek T.
      • Potharst-Sirag E.S.
      • Aarnoudse-Moens C.S.H.
      • van Wassenaer-Leemhuis A.G.
      Minor neurological dysfunction in five year old very preterm children is associated with lower processing speed.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ,
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ,
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ,
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ,
      • Janssen A.J.W.M.
      • Nijhuis-van der Sanden M.W.G.
      • Akkermans R.P.
      • Tissingh J.
      • Oostendorp R.A.B.
      • Kollée L.A.A.
      A model to predict motor performance in preterm infants at 5 years.
      ,
      • Zanudin A.
      • Gray P.H.
      • Burns Y.
      • Danks M.
      • Watter P.
      • Poulsen L.
      Perinatal factors in non-disabled ELBW school children and later performance.
      ], with one third of the studies reporting problems in more than half of the children aged 4.9 to 12–13 years of age. Among controls, the prevalence of motor problems in studies using the Movement ABC or Movement ABC-2 varied from 0 to 8.0% (5th percentile) [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ,
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ,
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ] and from 0 to 14.0% (15th percentile) [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ,
      • Rademaker K.J.
      • et al.
      Larger corpus callosum size with better motor performance in prematurely born children.
      ,
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ,
      • Flamand V.H.
      • Nadeau L.
      • Schneider C.
      Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ]. Using the BOTMP, prevalence of motor problems in VP/VLBW individuals was 15.0–16.1% in studies with cut-off at the 5th percentile or −2 SD [
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ,
      • Hack M.
      • et al.
      Chronic conditions, functional limitations, and special health care needs of school-aged children born with extremely low-birth-weight in the 1990s.
      ,
      • Holsti L.
      • Grunau R.V.E.
      • Whitfield M.F.
      Developmental coordination disorder in extremely low birth weight children at nine years.
      ,
      • Wocadlo C.
      • Rieger I.
      Motor impairment and low achievement in very preterm children at eight years of age.
      ] and 31.3–51.0% in studies with cut-off at the 15th percentile or −1 SD [
      • Hack M.
      • et al.
      Chronic conditions, functional limitations, and special health care needs of school-aged children born with extremely low-birth-weight in the 1990s.
      ,
      • Holsti L.
      • Grunau R.V.E.
      • Whitfield M.F.
      Developmental coordination disorder in extremely low birth weight children at nine years.
      ,
      • Wocadlo C.
      • Rieger I.
      Motor impairment and low achievement in very preterm children at eight years of age.
      ]. The prevalence among controls in studies using the BOTMP varied from 0 to 6.0% (≤5th percentile or <-2 SD) and from 5.0 to 10.0% (<15th percentile or <-1 SD) [
      • Hack M.
      • et al.
      Chronic conditions, functional limitations, and special health care needs of school-aged children born with extremely low-birth-weight in the 1990s.
      ,
      • Holsti L.
      • Grunau R.V.E.
      • Whitfield M.F.
      Developmental coordination disorder in extremely low birth weight children at nine years.
      ].
      Fig. 2
      Fig. 2Prevalence of motor problems in VP/VLBW individuals assessed by using various motor tests and cut-offs in the order of years of birth of the study participants. No controls <5th percentile. §No controls ≤5th or 15th percentile. BOTMP: Bruininks-Oseretsky Test of Motor Proficiency; Movement ABC/ABC-2: Movement Assessment Battery for Children/Second edition; VLBW: Very low birth weight; VP: Very preterm; SD: Standard deviation.

      3.5 Prevalence of domain-specific problems in VP/VLBW individuals without CP

      Manual dexterity problems were present in 3.0% of 5-year-old VP children [
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ] using a −2 SD cut-off and in 16% of VLBW adolescents [
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ] using the 5th percentile cut-off on the Movement ABC-2/ABC (data not shown). The prevalence ranged from 21.4% [
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ] using a −1 SD cut-off to 49% in 9-year-old VLBW children using the 15th centile cut-off [
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ]. Prevalence of problems in ball skills ranged from 2.5% <-2 SD [
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ] to 26% < 15th percentile [
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ], whereas prevalence of balance problems ranged from 3.0% <-2 SD [
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ] to 35% < 15th percentile [
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ]. In VLBW adolescents, the odds were significantly increased for having manual dexterity and balance problems <5th and 15th percentile, but not for problems in ball skills [
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ]. However, in a Swedish national cohort, not only were the odds of having manual dexterity (adjusted OR: 8.44; 99%CI: 3.64–19.57) and balance problems (OR: 4.24; 99%CI: 1.84–9.72) in 6.5-year-old EP children increased, but the odds were also significantly increased for problems in ball skills (OR: 4.93; 99%CI: 2.26–10.77) [
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ].
      The prevalence of ZNA pure motor scores <10th percentile was similar (24% and 25%) at 6 [
      • Seitz J.
      • Jenni O.G.
      • Molinari L.
      • Caflisch J.
      • Largo R.H.
      • Latal Hajnal B.
      Correlations between motor performance and cognitive functions in children born < 1250 g at school age.
      ] and 10 years [
      • Natalucci G.
      • et al.
      Development of neuromotor functions in very low birth weight children from six to 10 years of age: patterns of change.
      ] in the same VLBW cohort. Poor fine motor scores occurred in 38% at 6 years, and 17% at 10 years, while poor gross motor scores occurred in 26% at 6 years and 34% at 10 years. Rates of poor static balance were rather similar at 6 (20%) and 10 years (18%) [
      • Natalucci G.
      • et al.
      Development of neuromotor functions in very low birth weight children from six to 10 years of age: patterns of change.
      ]. Holsti et al., 2002 [
      • Holsti L.
      • Grunau R.V.E.
      • Whitfield M.F.
      Developmental coordination disorder in extremely low birth weight children at nine years.
      ] reported that of the 9-year-old ELBW children that were classified as having DCD based on BOTMP scores <-1 SD on the gross motor, fine motor or battery composite, 57% had a low gross motor composite score, 16% had a low fine motor composite score and 27% had low scores in both gross and fine motor composite areas.

      3.6 Risk factors for poor motor outcomes in VP/VLBW individuals without CP

      Twenty-five articles reported on risk factors for poor motor outcomes. Several studies found that boys performed worse than girls [
      • Davis N.M.
      • Ford G.W.
      • Anderson P.J.
      • Doyle L.W.
      Victorian Infant Collaborative Study Group, Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants.
      ,
      • Marlow N.
      • Hennessy E.M.
      • Bracewell M.A.
      • Wolke D.
      EPICure Study Group
      Motor and executive function at 6 years of age after extremely preterm birth.
      ,
      • Leversen K.T.
      • et al.
      Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm.
      ,
      • Zwicker J.G.
      • Yoon S.W.
      • Mackay M.
      • Petrie-Thomas J.
      • Rogers M.
      • Synnes A.R.
      Perinatal and neonatal predictors of developmental coordination disorder in very low birthweight children.
      ,
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ,
      • Janssen A.J.W.M.
      • Nijhuis-van der Sanden M.W.G.
      • Akkermans R.P.
      • Tissingh J.
      • Oostendorp R.A.B.
      • Kollée L.A.A.
      A model to predict motor performance in preterm infants at 5 years.
      ,
      • Zanudin A.
      • Gray P.H.
      • Burns Y.
      • Danks M.
      • Watter P.
      • Poulsen L.
      Perinatal factors in non-disabled ELBW school children and later performance.
      ], but one study reported poorer outcome for girls [
      • Powls A.
      • Botting N.
      • Cooke R.W.
      • Marlow N.
      Motor impairment in children 12 to 13 years old with a birthweight of less than 1250 g.
      ] and some found no effect of sex [
      • Flamand V.H.
      • Nadeau L.
      • Schneider C.
      Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ,
      • Holsti L.
      • Grunau R.V.E.
      • Whitfield M.F.
      Developmental coordination disorder in extremely low birth weight children at nine years.
      ,
      • Wocadlo C.
      • Rieger I.
      Motor impairment and low achievement in very preterm children at eight years of age.
      ].
      Apart from sex, lower birth weight [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Zwicker J.G.
      • Yoon S.W.
      • Mackay M.
      • Petrie-Thomas J.
      • Rogers M.
      • Synnes A.R.
      Perinatal and neonatal predictors of developmental coordination disorder in very low birthweight children.
      ,
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ,
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ], small for gestational age [
      • Torrioli M.G.
      • et al.
      Perceptual-motor, visual and cognitive ability in very low birthweight preschool children without neonatal ultrasound abnormalities.
      ,
      • Leversen K.T.
      • et al.
      Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm.
      ,
      • Tanis J.C.
      • et al.
      Functional outcome of very preterm-born and small-for-gestational-age children at school age.
      ] or poor fetal growth [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ], lower gestational age [
      • Leversen K.T.
      • et al.
      Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm.
      ,
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ,
      • Janssen A.J.W.M.
      • Oostendorp R.A.B.
      • Akkermans R.P.
      • Steiner K.
      • Kollée L.A.A.
      • Nijhuis-van der Sanden M.W.G.
      High variability of individual longitudinal motor performance over five years in very preterm infants.
      ,
      • Janssen A.J.W.M.
      • Nijhuis-van der Sanden M.W.G.
      • Akkermans R.P.
      • Tissingh J.
      • Oostendorp R.A.B.
      • Kollée L.A.A.
      A model to predict motor performance in preterm infants at 5 years.
      ] but also increasing gestational age given a birth weight <1000g [
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ] were reported as risk factors for motor problems. Among obstetric and maternal risk factors, premature rupture of membranes [
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ], lower maternal age at childbirth [
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ], mother being unemployed [
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ] and poorer family environment resources [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ] were associated with poorer motor outcome, whereas some reported that mother's education [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ,
      • Janssen A.J.W.M.
      • Nijhuis-van der Sanden M.W.G.
      • Akkermans R.P.
      • Tissingh J.
      • Oostendorp R.A.B.
      • Kollée L.A.A.
      A model to predict motor performance in preterm infants at 5 years.
      ], father's education [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ], income [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ] or socioeconomic status [
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ] were not. A long list of neonatal risk factors, such as lower Apgar score after 5 min, neonatal septicaemia and abnormal movements [
      • Marlow N.
      • Roberts B.L.
      • Cooke R.W.
      Motor skills in extremely low birthweight children at the age of 6 years.
      ], neonatal lung disease [
      • Zanudin A.
      • Gray P.H.
      • Burns Y.
      • Danks M.
      • Watter P.
      • Poulsen L.
      Perinatal factors in non-disabled ELBW school children and later performance.
      ], retinopathy of prematurity [
      • Goyen T.-A.
      • Lui K.
      Developmental coordination disorder in ‘apparently normal’ schoolchildren born extremely preterm.
      ,
      • Leversen K.T.
      • et al.
      Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ], postnatal corticosteroids [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ,
      • Short E.J.
      • et al.
      Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.
      ,
      • Zwicker J.G.
      • Yoon S.W.
      • Mackay M.
      • Petrie-Thomas J.
      • Rogers M.
      • Synnes A.R.
      Perinatal and neonatal predictors of developmental coordination disorder in very low birthweight children.
      ,
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ,
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ], bronchopulmonal dysplasia (BPD) [
      • Short E.J.
      • et al.
      Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.
      ,
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ,
      • Dewey D.
      • et al.
      Assessment of developmental coordination disorder in children born with extremely low birth weights.
      ], and duration on supplemental oxygen [
      • Short E.J.
      • et al.
      Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.
      ] and mechanical ventilation [
      • Bolk J.
      • Farooqi A.
      • Hafström M.
      • Åden U.
      • Serenius F.
      Developmental coordination disorder and its association with developmental comorbidities at 6.5 Years in apparently healthy children born extremely preterm.
      ,
      • Wocadlo C.
      • Rieger I.
      Motor impairment and low achievement in very preterm children at eight years of age.
      ], neonatal surgery [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ], white matter abnormalities [
      • Spittle A.J.
      • et al.
      Neonatal white matter abnormality predicts childhood motor impairment in very preterm children.
      ], decreased brain volumes at term [
      • Setänen S.
      • Lehtonen L.
      • Parkkola R.
      • Matomäki J.
      • Haataja L.
      The motor profile of preterm infants at 11 y of age.
      ], intraventricular haemorrhage (IVH) [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ,
      • Janssen A.J.W.M.
      • Nijhuis-van der Sanden M.W.G.
      • Akkermans R.P.
      • Tissingh J.
      • Oostendorp R.A.B.
      • Kollée L.A.A.
      A model to predict motor performance in preterm infants at 5 years.
      ] and cystic periventricular leukomalacia (PVL) [
      • Spittle A.J.
      • Cameron K.
      • Doyle L.W.
      J. L. Cheong, and Victorian Infant Collaborative Study group, Motor impairment trends in extremely preterm children: 1991-2005.
      ] were reported as risk factors for motor problems in the reviewed articles.

      4. Discussion

      We identified 38 original publications fulfilling the inclusion criteria. Of them, 23 were not part of the three previous reviews of VP/VLBW children [
      • Edwards J.
      • et al.
      Developmental coordination disorder in school-aged children born very preterm and/or at very low birth weight: a systematic review.
      ,
      • de Kieviet J.F.
      • Piek J.P.
      • Aarnoudse-Moens C.S.
      • Oosterlaan J.
      Motor development in very preterm and very low-birth-weight children from birth to adolescence: a meta-analysis.
      ,
      • FitzGerald T.L.
      • Kwong A.K.L.
      • Cheong J.L.Y.
      • McGinley J.L.
      • Doyle L.W.
      • Spittle A.J.
      Body structure, function, activity, and participation in 3- to 6-year-old children born very preterm: an ICF-based systematic review and meta-analysis.
      ], as we included more recent publications and articles reporting both continuous motor scores and/or prevalence of motor problems assessed by a wider variety of tests. Age at assessment varied from our lower limit of 5 years and up to 14 years, with the exception of the Norwegian NTNU cohort also assessed at 22.5 years [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ]. All studies came from high-income countries except two studies from a middle-income country [
      • Oliveira G.E.
      • Magalhães L.C.
      • Salmela L.F.T.
      Relationship between very low birth weight, environmental factors, and motor and cognitive development of children of 5 and 6 years old.
      ,
      • Moreira R.S.
      • Magalhães L.C.
      • Dourado J.S.
      • Lemos S.M.A.
      • Alves C.R.L.
      Factors influencing the motor development of prematurely born school-aged children in Brazil.
      ].
      There were substantial differences between VP/VLBW children and controls across all ages. Typical mean differences in continuous scores were in the order of magnitude of 1 SD. In studies that reported subdomain scores, differences were present across all motor domains, as reported by de Kieviet et al., 2009 [
      • Edwards J.
      • et al.
      Developmental coordination disorder in school-aged children born very preterm and/or at very low birth weight: a systematic review.
      ], with increased risk of poor manual dexterity/fine motor function, ball skills and balance/gross motor function. In accordance with Edwards et al., 2011 [
      • Blank R.
      • et al.
      International clinical practice recommendations on the definition, diagnosis, assessment, intervention, and psychosocial aspects of developmental coordination disorder.
      ], the prevalences of motor problems were several-fold larger than those in controls, but with some uncertainty, partly because of low number of cases among term-born controls. There was no evidence that younger children had higher prevalence of motor problems, neither did it seem related to years of birth. Potential reasons for the wide variation in difference in mean scores and prevalence of problems may be related to differences in study designs and settings, selection and exclusion criteria, follow-up rates and applied test norms.
      These differences compare with differences in other key outcomes in VP/VLBW children and adults. Cognitive abilities have been extensively studied and remain 0.70 to 0.86 SD lower in VP/VLBW children than in controls [
      • Sentenac M.
      • et al.
      A tale of missing studies: defining very preterm populations for systematic reviews with meta-analysis..
      ]. Other examples include pulmonary airflow, showing a similar difference, 0.80 SD, in 1-s forced expiratory flow in VLBW adults [
      • Doyle L.W.
      • et al.
      Expiratory airflow in late adolescence and early adulthood in individuals born very preterm or with very low birthweight compared with controls born at term or with normal birthweight: a meta-analysis of individual participant data.
      ], whereas the difference in blood pressure is smaller, corresponding to 0.3 SD [
      • Hovi P.
      • et al.
      Blood pressure in young adults born at very low birth weight: adults born preterm international collaboration.
      ,
      • Hovi P.
      • et al.
      Ambulatory blood pressure in young adults with very low birth weight.
      ]. Together these numbers indicate that poorer motor skills, even without the presence of manifest CP, are an essential part of the “VP/VLBW phenotype” at least in childhood.
      There is little evidence on whether and to what extent poorer motor skills persist to adulthood. The only published study extending to adulthood is the Norwegian NTNU cohort [
      • Husby I.M.
      • Skranes J.
      • Olsen A.
      • Brubakk A.-M.
      • Evensen K.A.I.
      Motor skills at 23 years of age in young adults born preterm with very low birth weight.
      ], which suggests that the deficits in fine and gross motor skills in VLBW children persist to adulthood. While the mean differences with controls were relatively small in comparison with studies in childhood, the proportion of those with motor problems was similar to what was shown in the same cohort at 14 years of age [
      • Evensen K.A.I.
      • Vik T.
      • Helbostad J.
      • Indredavik M.S.
      • Kulseng S.
      • Brubakk A.-M.
      Motor skills in adolescents with low birth weight.
      ]. This paucity of evidence contrasts with the increasing research activity on other outcomes in adult VP/VLBW cohorts and may in part be due to a lack of assessment tools validated for young adults; we argue for incorporating motor outcomes in follow-up studies in these cohorts.
      Even though some other reviews have included all degrees of prematurity [
      • Allotey J.
      • et al.
      Cognitive, motor, behavioural and academic performances of children born preterm: a meta-analysis and systematic review involving 64 061 children.
      ,
      • Williams J.
      • Lee K.J.
      • Anderson P.J.
      Prevalence of motor-skill impairment in preterm children who do not develop cerebral palsy: a systematic review.
      ,
      • Moreira R.S.
      • Magalhães L.C.
      • Alves C.R.L.
      Effect of preterm birth on motor development, behavior, and school performance of school-age children: a systematic review.
      ,
      • Upadhyay R.P.
      • et al.
      Cognitive and motor outcomes in children born low birth weight: a systematic review and meta-analysis of studies from South Asia.
      ,
      • Bos A.F.
      • Van Braeckel K.N.J.A.
      • Hitzert M.M.
      • Tanis J.C.
      • Roze E.
      Development of fine motor skills in preterm infants.
      ], the majority of the included studies focused on VP/VLBW or more immature or smaller subgroups. Much of the improvement in VP/VLBW survival has been related to improvements in resource-intensive neonatal care units in high-resource settings. These typically also have follow-up and medical, social and educational support systems in place, which is reflected in the settings of the included studies. With improving prenatal and newborn care, survival of VP/VLBW infants is increasing also in lower-resource settings [
      • March of Dimes
      • PMNCH
      Save the children, WHO. Born Too Soon: The Global action report on preterm birth.
      ]. The published results may therefore reflect a conservative estimate in relation to these settings which may also have lower resources for follow-up and support.
      According to Spittle & Orton 2014 [
      • Spittle A.J.
      • Orton J.
      Cerebral palsy and developmental coordination disorder in children born preterm.
      ], all forms of motor impairment are associated with comorbidities. Thus, there is reason to believe that the motor problems seen in VP/VLBW children are part of more widespread brain pathology [
      • Skranes J.
      Is developmental coordination disorder in preterm children the motor phenotype of more widespread brain pathology?.
      ], and may act as an early biomarker for cognitive and behavioural problems later in childhood [
      • Skranes J.
      Is developmental coordination disorder in preterm children the motor phenotype of more widespread brain pathology?.
      ]. Motor and coordination problems in childhood and adolescence have been found to be associated with overall psychiatric problems in VLBW adults [
      • Lærum A.M.W.
      • et al.
      Psychiatric symptoms and risk factors in adults born preterm with very low birthweight or born small for gestational age at term.
      ], and elevated levels of inattention and symptoms of anxiety and depression in both ELBW and control adults [
      • Poole K.L.
      • Schmidt L.A.
      • Missiuna C.
      • Saigal S.
      • Boyle M.H.
      • Van Lieshout R.J.
      Motor coordination and mental health in extremely low birth weight survivors during the first four decades of life.
      ]. These co-occurrent problems may have a greater effect on quality of life, academic achievement and participation in extracurricular activities than the motor impairment itself [
      • Spittle A.J.
      • Orton J.
      Cerebral palsy and developmental coordination disorder in children born preterm.
      ]. Several studies have reported lower physical activity, sports participation and recreational activities among young adults born VP/VLBW [
      • Kajantie E.
      • et al.
      Adults born at very low birth weight exercise less than their peers born at term.
      ,
      • Rogers M.
      • Fay T.B.
      • Whitfield M.F.
      • Tomlinson J.
      • Grunau R.E.
      Aerobic capacity, strength, flexibility, and activity level in unimpaired extremely low birth weight (<or=800 g) survivors at 17 years of age compared with term-born control subjects.
      ,
      • Kaseva N.
      • et al.
      Lower conditioning leisure-time physical activity in young adults born preterm at very low birth weight.
      ,
      • Andersen L.G.
      • et al.
      Birth weight in relation to leisure time physical activity in adolescence and adulthood: meta-analysis of results from 13 nordic cohorts.
      ,
      • Dahan-Oliel N.
      • Mazer B.
      • Riley P.
      • Maltais D.B.
      • Nadeau L.
      • Majnemer A.
      Participation and enjoyment of leisure activities in adolescents born at ≤ 29 week gestation.
      ] or less than 34 weeks of gestation [
      • Tikanmäki M.
      • et al.
      Leisure time physical activity in young adults born preterm.
      ]. While these differences have usually not been seen in studies measuring physical activity by accelerometry [
      • Kaseva N.
      • et al.
      Objectively measured physical activity in young adults born preterm at very low birth weight.
      ], they are accompanied by findings of lower lean body mass [
      • Hovi P.
      • et al.
      Glucose regulation in young adults with very low birth weight.
      ] and physical fitness [
      • Rogers M.
      • Fay T.B.
      • Whitfield M.F.
      • Tomlinson J.
      • Grunau R.E.
      Aerobic capacity, strength, flexibility, and activity level in unimpaired extremely low birth weight (<or=800 g) survivors at 17 years of age compared with term-born control subjects.
      ,
      • Tikanmäki M.
      • et al.
      Physical fitness in young adults born preterm.
      ]. They may be a result of a vicious cycle where poor motor coordination have been suggested to play a key role, perhaps together with lower pulmonary airflow [
      • Doyle L.W.
      • et al.
      Expiratory airflow in late adolescence and early adulthood in individuals born very preterm or with very low birthweight compared with controls born at term or with normal birthweight: a meta-analysis of individual participant data.
      ] and poor visual acuity [
      • Evensen K.A.I.
      • Lindqvist S.
      • Indredavik M.S.
      • Skranes J.
      • Brubakk A.-M.
      • Vik T.
      Do visual impairments affect risk of motor problems in preterm and term low birth weight adolescents?.
      ]. This may lead to lower physical self-confidence and perceived physical ability [
      • Saigal S.
      • et al.
      Comparison of current health, functional limitations, and health care use of young adults who were born with extremely low birth weight and normal birth weight.
      ], together making physical activity less rewarding, leading to lower degrees of physical activity and may also aggravate the lower exercise capacity and lower lean body mass. Therefore, we believe that promotion of health-enhancing physical activity, with special reference to challenges in motor skills, has potential in improving the health of children and adults born VP/VLBW. Spittle & Orton 2014 [
      • Spittle A.J.
      • Orton J.
      Cerebral palsy and developmental coordination disorder in children born preterm.
      ] argue that a reliable diagnosis of motor impairment requires follow-up into childhood and is important to ensure that the appropriate intervention is implemented. Interventions that are activity-oriented and involve environmental support by family and significant others to facilitate participation across contexts are recommended [
      • Blank R.
      • et al.
      International clinical practice recommendations on the definition, diagnosis, assessment, intervention, and psychosocial aspects of developmental coordination disorder.
      ]. However, evidence regarding which interventions are most effective in improving motor outcomes is sparse and few studies have assessed long-term effects [
      • Spittle A.
      • Orton J.
      • Anderson P.J.
      • Boyd R.
      • Doyle L.W.
      Early developmental intervention programmes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants.
      ,
      • Hughes A.J.
      • Redsell S.A.
      • Glazebrook C.
      Motor development interventions for preterm infants: a systematic review and meta-analysis.
      ].
      Several studies reported neonatal risk and male sex as factors explaining part of the motor problems. These findings are supported by the review of Bos et al., 2013 [
      • Bos A.F.
      • Van Braeckel K.N.J.A.
      • Hitzert M.M.
      • Tanis J.C.
      • Roze E.
      Development of fine motor skills in preterm infants.
      ], who reported intrauterine growth restriction, inflammatory conditions and BPD as risk factors for fine motor skill impairments in preterm children. Furthermore, Linsell et al., 2016 [
      • Linsell L.
      • Malouf R.
      • Morris J.
      • Kurinczuk J.J.
      • Marlow N.
      Prognostic factors for cerebral palsy and motor impairment in children born very preterm or very low birthweight: a systematic review.
      ] reported IVH and/or PVL to be a prominent feature in the medical history of children not only developing CP, but also minor neurological dysfunctions.
      This review was based on a systematic literature search. We focused on children aged five years or older, whereas previous reviews also have included younger children. We excluded articles that included even mild degrees of CP, and we present both continuous motor test scores and prevalence of motor problems, as well as domain-specific test scores and problems. One reason for not performing a meta-analysis was the different methods used to assess motor skills. Although most studies used either the Movement ABC or Movement ABC-2, some reported mean (SD), whereas other reported median (IQR or range) scores, and different cut-offs were used to identify motor problems.

      4.1 Conclusion

      Including recent studies and excluding all degrees of manifest CP, we found that VP/VLBW individuals had poorer motor skills in terms of total test scores, domain-specific test scores and increased prevalence of total motor and domain-specific problems. There was a wide variability in results between studies, however it seemed not related to age or years of birth. The motor problems are present when the children generally no longer attend preterm-specific follow-up programs. Healthcare and education professionals should be aware of increased risk of such problems, to provide appropriate intervention, including environmental adjustments and understanding of their motor problems, to promote participation and reduce the impact on everyday activities and future health problems.

      4.2 Practice points

      • Children and young adults born very preterm or with very low birth weight have increased risk of poor motor skills in terms of total test scores and domain-specific test scores.
      • Healthcare and education professionals should be aware that these problems are manifest when the children generally no longer attend preterm-specific follow-up programs and provide appropriate interventions to reduce the impact on everyday life.

      4.3 Research agenda

      • Motor problems in the much larger groups of children born moderate and late preterm in high and low resource settings.
      • Persistence of motor problems and their significance in later adult life.
      • The role of motor problems in developing physical activity habits and consequently physical fitness.
      • Interventions and their effectiveness long term.

      Funding sources

      The work of Drs. Evensen, Tikanmäki, Haaramo and Kajantie was supported by funding from the European Union's Horizon 2020 Research and Innovation Program RECAP Preterm Project (grant no. 733280 ). The work of Dr. Ustad was supported by grant from The Liaison Committee for Education, Research and Innovation in Central Norway . Dr. Evensen has received grant from the Liaison Committee of St. Olavs Hospital and NTNU, Dr. Haaramo from Norface DIAL Premlife project and Dr. Kajantie from Academy of Finland (grant no. 315690 ), Signe and Ane Gyllenberg Foundation and Foundation for Pediatric Research , Yrjö Jahnsson Foundation , Juho Vainio Foundation , Finnish Foundation for Cardiovascular Research , Novo Nordisk Foundation and Finnish Diabetes Research Foundation .

      Declaration of competing interest

      None declared.

      Appendix A. Search terms for MEDLINE database using the PubMed search engine

      (“premature birth"[All Fields] OR “premature infant"[All Fields] OR “born premature"[All Fields] OR “preterm"[All Fields] OR “very preterm"[All Fields] OR “extremely preterm"[All Fields] OR “low birth weight"[All Fields] OR “very low birth weight"[All Fields] OR “extremely low birth weight"[All Fields] OR “Infant, Premature"[All Fields] OR “Infant, Low Birth Weight"[All Fields] OR “Infant, Very Low Birth Weight"[All Fields] OR “Obstetric Labor, Premature"[All Fields] OR “prematurity"[All Fields])
      AND
      (“movement"[All Fields] OR “motor skills"[All Fields] OR “motor function"[All Fields] OR “motor performance"[All Fields] OR “motor impairment"[All Fields] OR “motor delay"[All Fields] OR “motor deficit"[All Fields] OR “motor problems"[All Fields] OR “motor disorders"[All Fields] OR “developmental coordination disorder"[All Fields] OR “DCD"[All Fields] OR “fine motor"[All Fields] OR “gross motor"[All Fields] OR “manual dexterity"[All Fields] OR “hand function"[All Fields] OR “ball skills"[All Fields] OR “balance skill"[All Fields] OR “balance function"[All Fields] OR “static balance"[All Fields] OR “dynamic balance"[All Fields] OR “postural control"[All Fields] OR “postural stability"[All Fields] OR “motor speed"[All Fields] OR “Movement Assessment Battery for Children"[All Fields] OR “Movement ABC"[All Fields] OR “MABC"[All Fields] OR “MABC-2"[All Fields] OR “Bruininks-Oseretsky Test of Motor Proficiency"[All Fields] OR “BOTMP"[All Fields] OR “BOT-2"[All Fields] OR “Motor Skills Disorders"[All Fields])

      Appendix. B Table 1. Standardised and norm-based motor tests to describe motor skills and/or identify motor problems in the included articles

      Tabled 1
      TestAge rangeItems included in the testScoring
      Movement Assessment Battery for Children (Movement ABC) [
      • Henderson S.E.
      • Sugden D.A.
      Movement Assessment Battery for Children. Manual.
      ]
      4-12 yEight items in three subscores; manual dexterity (three items), ball skills (two items), static/dynamic balance (three items).Raw scores converted to standard scores on a 6-point scale (0–5; 0 being optimal score) for each item and summarised to a total impairment score (maximum 40). Scores <5th and <15th percentile indicate definite and borderline motor problems.
      Movement Assessment Battery for Children-2 Second edition (Movement ABC-2) [
      • Henderson S.E.
      • Sugden D.A.
      • Barnett A.L.
      Movement Assessment Battery for Children-2. Examiner's manual.
      ]
      3-16 yEight items in three subscores; manual dexterity (three items), aiming and catching (two items), balance (three items).Raw scores converted to standard scores 1–19 for each item (higher indicating better skills) and summarised to a total score (maximum 152). Scores ≤5th and ≤15th percentile denote a significant movement difficulty or suggest the child is at risk of having a movement difficulty.
      Test of Motor Impairment (TOMI) [
      • Stott D.
      • Moyes F.
      • Henderson S.
      Test of Motor Impairment.
      ]
      5-12 yEight items in three subscores; manual dexterity (three items), ball skills (two items), static and dynamic balance (three items).Scored on a 3-point scale (0 = no problems, 1 = some problems, 2 = difficulties) and summarised to a total score (maximum 16).
      Bruininks-Oseretsky Test of Motor Proficiency (BOTMP) [
      • Bruininks R.H.
      Bruininks-Oseretsky Test of Motor Proficiency: examiner's manual. Circle pines.
      ]
      4.5–14.5 yLong Form: 46 items in eight subtests; gross motor composite (four subtests), fine motor composite (three subtests) and battery composite (one subtest). Short Form: 14 items from the eight subtests.Scoring system varies with each item, ranging from a 2-point (pass/fail) to a 16-point scale. Raw scores converted to a numerical point score and composite scores expressed as centile rank, z-score, T score (mean 50; SD 10), stanine or age-equivalent.
      Körperkoordinationstest für Kinder (KTK) [
      • Weindrich D.
      • Jennen-Steinmetz C.
      • Laucht M.
      • Schmidt M.H.
      Late sequelae of low birthweight: mediators of poor school performance at 11 years.
      ,
      • Keller H.
      • Ayub B.V.
      • Saigal S.
      • Bar-Or O.
      Neuromotor ability in 5- to 7-year-old children with very low or extremely low birthweight.
      ]
      5-14 yFour tasks; walking backward on beams of decreasing width, jumping with each leg separately over an increasing height (number of foam plates), jumping sideways with both feet and moving across the floor by stepping from one plate on a second plate, then relocating the first plate before taking the next step and so on.Performances converted to a standard score, or motor quotient (MQ). A MQ between 90 and 110 represents normal coordination, while scores <80 indicate deficiencies in motor ability.
      Zurich Neuromotor Assessment (ZNA) [
      • Largo R.H.
      • et al.
      Neuromotor development from 5 to 18 years. Part 1: timed performance.
      ,
      • Largo R.H.
      • Caflisch J.A.
      • Hug F.
      • Muggli K.
      • Molnar A.A.
      • Molinari L.
      Neuromotor development from 5 to 18 years. Part 2: associated movements.
      ]
      5-18 yFive components; pure motor tasks, adaptive fine motor, adaptive gross motor, static balance and associated movements.Raw scores summarised to standard components and expressed as z-scores. Scores <10th percentile indicate abnormal performance.
      High-Level Mobility Assessment Tool (HiMAT) [
      • Williams G.
      • Morris M.
      • Greenwood K.
      • Goldie P.
      • Robertson V.
      High-level Mobility Assessment Tool for traumatic brain injury. HiMAT user manual. Melbourne: school of physiotherapy.
      ]
      >13 y13 items; walk, walk backwards, walk on toes, walk over obstacle, run, skip, hop forward, bound and walk up/down stairs.Raw scores are converted to a score on a 5-point scale (0–4), except stair items on a 6-point scale (0–5; higher score indicates better function). Maximal score of 54.
      Grooved Pegboard (GP) [
      ]
      >5 yInserting 25 pegs, one at a time, into keyhole-shaped holes with various orientations in a 5 × 5 matrix. Dominant and non-dominant hand are tested.Raw scores consist of time in seconds to complete the board and number of drops for each hand. Age-specific norms.
      Purdue Pegboard [
      ]]
      5-89 yPlacing as many pins as possible in the holes, within a 30 s time period. Preferred hand, non-preferred hand and both hands together are tested.Raw scores consist of number of pins inserted within the 30 s time period for each hand. Score for the bimanual condition consists of the total number of pairs of pins inserted.

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