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Review |

Neurodevelopmental Outcomes at 4 to 8 Years of Children Born at 22 to 25 Weeks’ Gestational Age:  A Meta-analysis FREE

Gregory P. Moore, MD, FRCPC1,2,3; Brigitte Lemyre, MD, FRCPC1,2,3; Nick Barrowman, PhD4; Thierry Daboval, MD, FRCPC1,2,3
[+] Author Affiliations
1Department of Pediatrics, Division of Neonatology, Children’s Hospital of Eastern Ontario, Ottawa, Ontario, Canada
2Department of Obstetrics and Gynecology, Division of Newborn Care, The Ottawa Hospital, General Campus, Ottawa, Ontario, Canada
3Department of Pediatrics, University of Ottawa, Ottawa, Ontario, Canada
4Children’s Hospital of Eastern Ontario Research Institute, Ottawa, Ontario, Canada
JAMA Pediatr. 2013;167(10):967-974. doi:10.1001/jamapediatrics.2013.2395.
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Published online

Importance  Many centers delivering infants at 22 to 25 weeks’ gestation have limited data regarding their outcomes. A meta-analysis of the 4- to 8-year neurodevelopmental outcomes and exploration of the limitations of meta-analysis would aid physicians and parents to plan care for these infants.

Objectives  To determine the rate of moderate to severe and severe neurodevelopmental impairment by gestational age in extremely preterm survivors followed up between ages 4 and 8 years, as well as to determine whether there is a significant difference in impairment rates between the successive weeks of gestation of survivors.

Evidence Review  A peer-reviewed search strategy obtained English-language publications from MEDLINE In-Process & Other Non-Indexed Citations, MEDLINE, and EMBASE. Personal files and reference lists from identified articles were searched. Contemporary cohorts were obtained by restriction to those published after 2004. Inclusion criteria were prospective cohort studies, follow-up rate of 65% or more, use of standardized testing or classification for impairment, reporting by gestation, and meeting prespecified definitions of impairment. We excluded randomized clinical trials, highly selective cohorts, consensus statements, and reviews. Of 1771 identified records, 89 full-text publications were assessed for eligibility. Using the full text of each publication, 2 authors independently followed a 2-step procedure. First, they determined that 9 studies met inclusion criteria. Next, they extracted data using a structured data collection form. Investigators were contacted for data clarification.

Results  All extremely preterm infant survivors have a substantial likelihood of developing moderate to severe impairment. Wide confidence intervals at the lower gestations (eg, at 22 weeks, 43% [95% CI, 21%-69%]; heterogeneity I2, 0%) and high heterogeneity at the higher gestations (eg, at 25 weeks, 24% [95% CI, 17%-32%]; I2, 66%) limit the results. There was a statistically significant absolute decrease in moderate to severe impairment between each week of gestation (6.5% [95% CI, 2%-11%]).

Conclusions and Relevance  Knowledge of these data, including the limitations, should facilitate discussion during the shared decision-making process about care plans for these infants, particularly in centers without their own data. More prospective, high-quality, complete cohorts are needed.

Figures in this Article

A common but difficult task for obstetricians, pediatricians, and neonatologists in developed countries is providing parents with meaningful information during shared decision-making (SDM) about their infant’s care plan when faced with the possibility that their child may be an extremely preterm infant (EPI) born at the edge of viability. In developed nations and hereafter in this article, EPIs are considered to be infants born between 22 weeks +0 days and 25 weeks +6 days’ gestational age (GA).15 For many parents, the chance of their EPI surviving with long-term neurodevelopmental impairment (NDI) is a deciding factor, possibly more important than survival,6 when choosing whether they will proceed with intensive care or palliative care at the time of their EPI’s birth.79

Data on NDI provide part of the base8 from which to initiate the SDM process,10,11 but multiple reasons limit their overall usefulness.6,1219 Physicians must recognize these limitations and discuss them with parents.20 Because the rates of NDI are center dependent, one solution to overcome some of the issues is to simply use center-specific outcomes.1,3,4,14 This is useful for larger centers with databases and follow-up programs. However, some centers that routinely care for EPIs or that deliver EPIs unexpectedly would not have reliable local data to discuss with parents.

Currently, there are no clear, unified contemporary data, such as a meta-analysis, on the NDI rates of EPIs at age 4 to 8 years. Assessing NDI at 4 to 8 years, rather than earlier, is vital because assessments at a younger age are likely to overestimate NDI rates.2123 Several medical organizations1,3 suggest that a compilation of high-quality, contemporary, generalizable data, with the fewest possible limitations, will guide physicians in providing comprehensive information to facilitate parents’ involvement in the SDM process.

The primary objective of our study was to determine the rate of moderate to severe and severe NDI by GA in EPI survivors followed up between ages 4 and 8 years. The secondary objective was to determine whether there is a statistically significant difference in NDI rates between GA weeks of EPI survivors. We hypothesized that there would be a significant decrease with increasing GA.

The recommendations of the Meta-analysis of Observational Studies in Epidemiology Group24 directed the methodology for our meta-analysis.

After consultation with one author (G.P.M.), a search strategy was created and run. It was developed in MEDLINE and peer reviewed prior to translation to EMBASE (eAppendix 1 in the Supplement).25 The databases searched were Ovid MEDLINE In-Process & Other Non-Indexed Citations; and Ovid MEDLINE 1948 to May week 3, 2012; and Ovid EMBASE 1980 to 2012, week 21. The search was limited to English-language material published after 2004, ensuring that cohorts with neonates born in 1995 or later (when contemporary neonatal care,17 including antenatal corticosteroids, surfactant, and improved nutrition,26 was routinely available) made up the 4- to 8-year NDI follow-up results.

The search was limited using 2 previously developed filters, the Cochrane Highly Sensitive Search Strategy for controlled trials27 and the Clinical Evidence filter to identify cohort studies (available at http://clinicalevidence.bmj.com/ceweb/about/search_filters.jsp). Additional articles and conference proceedings were sought from the authors’ (G.P.M., B.L., and T.D.) personal files and the references of obtained articles.

Titles were initially screened followed by the selected abstracts. Two authors (G.P.M./B.L. or G.P.M./T.D.) independently performed each stage of screening. Full-text articles or conference proceedings were then assessed in detail for eligibility by 2 authors (G.P.M./B.L., G.P.M./T.D., or B.L./T.D.) to minimize extraction error. A standardized data collection form (available upon request) was used; it included geography, type of neonatal unit (inborn/outborn/both), basic demographics, GAs assessed, article type, quality of outcome assessments, and survival, follow-up, and NDI rates (defined as n divided by N, where n indicates the number of survivors assessed at follow-up who have a specified NDI and N indicates the number of survivors assessed at follow-up for the specified NDI). Each article had a form completed independently by 2 authors (G.P.M./T.D., T.D./B.L., or B.L./G.P.M.) to minimize extraction error. In the event of any discord between authors, a third author assisted until consensus was reached.

One author (G.P.M.) attempted to contact the investigators via e-mails during a 9-month period if the data in the publication were not extractable in the necessary form for inclusion in the analysis. The same author assessed data received from contacted investigators to ensure there were no obvious errors.

To ensure the highest possible quality of observational data, several measures were used. Included studies had to meet the following criteria: cohort studies (with or without a control group made up of term infants), prospective data collection,28 follow-up rate of 65% or more of survivors aged 4 to 8 years, and use of standardized testing methods2935 for cognition and classification systems (or descriptions of functional impact) for cerebral palsy,36 visual impairment, or hearing impairment. To maximize uniformity by avoiding the wide variations in possible NDI definitions14 and allow for acceptable pooling of the data, the reported NDI had to meet our prespecified definitions. The definitions were selected for their frequent use by groups reporting on EPI outcomes3739 as well as their clinical relevance for families.40,41 Severe NDI, likely to make a child highly dependent on caregivers, was defined as an IQ score more than 3 SDs below the mean, nonambulant cerebral palsy (Gross Motor Functional Classification System, 4-5),36 no useful vision (worse than 20/200), or no useful hearing despite amplification. Moderate NDI was defined as an IQ score 2 to 3 SDs below the mean, ambulant cerebral palsy (Gross Motor Functional Classification System, 2-3), little useful vision (worse than 20/40), or hearing restored with amplification. Infants were classified as having moderate to severe NDI if they met 1 or more of these criteria. We also reported severe NDI rates separately because, in our experience, expectant parents frequently use the information during SDM.

The rates of NDI had to be based on GA rather than birth weight because GAs are more applicable for antenatal consultations, avoid the inclusion of more mature but growth-restricted infants, and are the preferred method of reporting outcomes.1,16,18,19 Completed weeks of gestation defined the GA. For cohorts with multiple publications, we included only the results for follow-up at 4 to 8 years. Finally, we excluded randomized clinical trials, highly selective cohorts (eg, reports on only infants with intrauterine growth restriction), consensus statements, and review articles.

Statistical Analysis

For the primary objective, rates of NDI were transformed using a logit transformation and then pooled across studies using the Dersimonian-Laird random-effects method.42 In studies in which the rate was 0% or 100%, before computing the logit, 0.5 was added to the numerator and 1 was added to the denominator. The weighted contribution of each study was assessed by the Dersimonian-Laird procedure. Heterogeneity between proportions was assessed using the Higgins I2 statistic.43 Confidence intervals for individual proportions were obtained using the Wilson score method. No attempt was made to statistically assess publication bias since it is not clear how publication bias could operate for cohort studies that report on proportions without a true comparison group; we note that cohorts with poorer NDI outcomes may be less likely to be published. Additionally, to assess for possible bias involving studies that did not include a term-control group, studies with this group were pooled separately from those without one. A z-test at each GA compared the pooled estimates from the studies with and without a term-control group. The Holm method was used to adjust the P values from the multiple z-tests.44

For the secondary objective, the absolute percent change in NDI rate with each week of GA within each study was first estimated using the slope from a linear binomial model. The change with GA was estimated within each study so that infants were directly compared only with others from the same center. In one case, there was convergence to a boundary of the parameter space where the probability is zero; this can occur because of the restriction of the parameter space in a linear binomial model.45 This was overcome using the COPY method of Deddens and Petersen.46 Slopes were pooled42 and heterogeneity was assessed.43 Publication bias was not assessed because the primary objective of the individual cohorts was not to assess the change in NDI rate with each week of GA; therefore, it seems implausible that this should influence the probability of publication of such studies.

All calculations were performed using R, version 2.15.1.47 Pooling was performed using the meta-package.48

The search strategy yielded 2448 records, and our gray literature search yielded 53 records. After the screening and eligibility assessment, 9 studies met the criteria for inclusion 49(Figure 1).

Place holder to copy figure label and caption
Figure 1.
Flow of Information Through Systematic Review

The Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines were used for selection and screening of data.49

Graphic Jump Location

The included studies are described in the Table. Five studies3739,50,54 had a term-control group. There was no statistically significant difference between the moderate to severe NDI rates of children born at 22 weeks (P = .70), 23 weeks (P = .16), and 25 weeks (P = .41) of studies using a control group vs those not using a control group. There was a statistically significant difference at 24 weeks (P = .03); however, this was not significant on adjustment for multiple testing.

Table Graphic Jump LocationTable.  Description of Included Studies Including Assessment of Study Quality

Lack of data clarification from 2 of the investigators resulted in the inability to determine the rates of severe NDI of the children born at 24 and 25 weeks’ GA50,53 (eAppendix 2 in the Supplement). One cohort did not include children born at 22 weeks’ GA.54 Several cohorts had no GA survivors at 22-weeks.5052

The rates of moderate to severe and severe NDI for each successive GA week are shown in Figure 2. Moderate to severe NDI rates demonstrated increasing heterogeneity as the GA increased, and small sample sizes for the lowest GAs resulted in wide confidence intervals around the estimates. Across these meta-analyses, the maximum mean weighted contribution of a study toward moderate to severe NDI rates was 52%55 at 22 weeks’ GA, 21%37 at 23 weeks’ GA, 16%37 at 24 weeks’ GA, and 15%37 at 25 weeks’ GA.

Place holder to copy figure label and caption
Figure 2.
Random-Effects Meta-analysis of Moderate to Severe and Severe Neurodevelopmental Impairment Rates

Data markers indicate mean value; whiskers, 95% CI; and diamonds, pooled estimate (width of the diamond represents the 95% CI).

Graphic Jump Location

The meta-analysis results of comparing the difference in the rate of moderate to severe and severe NDI between each successive GA week are shown in Figure 3. The risk of moderate to severe NDI decreased for each additional GA week (6% [95% CI, 1.7%-10.3%]). Severe NDI did not significantly decrease with each GA week.

Place holder to copy figure label and caption
Figure 3.
Random-Effects Meta-analysis of the Risk Difference of Neurodevelopmental Impairment for Each Additional Week of Gestational Age (GA)

Data markers indicate mean value; whiskers, 95% CI; and diamonds, pooled estimate (width of the diamond represents the 95% CI).

Graphic Jump Location

To our knowledge, this meta-analysis of the NDI rates in EPIs at age 4 to 8 years is the first such report in the medical literature. Through contact with nearly every investigator of the publications we used, we were able to include unpublished information in the meta-analysis. Our results provide novel pooled data for some of the most clinically important outcomes for EPI survivors, along with insight into the limitations of data on their long-term NDI rates. Most important, we demonstrate that there is a statistically significant decrease in moderate to severe NDI between each successive EPI week of gestation (Figure 3). However, regardless of the GA at birth, all EPI survivors have a notable likelihood of developing moderate to severe NDI (Figure 2).

Two recent systematic reviews56,57 examined EPI outcomes, including their rates of NDI. Baron and Rey-Casserly56 reviewed cognitive research articles published since 1970 but did not contact investigators.24 They included 18 studies on infants born in 1995 or later; the cohorts’ diversity, frequent follow-up at less than 4 years,2123 uncertain follow-up rates, and occasional reporting by birth weight16,18,19 hampered their ability to comment on the results with precision. Lorenz57 included 10 articles involving infants born after 1994 with a follow-up rate of at least 70%. A lack of reporting by each respective GA week, no attempt to contact the investigators,24 and inclusion of cohorts with suboptimal neurodevelopmental assessments limit the usefulness of the findings. Given the problems with these reviews, we believe our results offer higher-quality data to assist physicians who do not have center-specific data to discuss with parents during the SDM process.

In addition, 2 meta-analyses within the last 11 years reported more broadly on outcomes of children born preterm.58,59 Bhutta and colleagues58 assessed 31 studies dealing with only cognitive and behavioral outcomes at 5 years or longer in children who were born preterm. This publication was limited by no attempt to contact investigators,24 inclusion of cohorts that excluded severely impaired survivors, lack of clear GA-based data, and limited generalizability for the contemporary EPI population (included infants born between 1975 and 1988 and few were EPIs). Mwaniki et al59 reviewed multiple factors that can result in NDI, one of which was prematurity. The authors included 13 studies involving newborns with birth weight less than 1501 g; lack of GA-based data and inclusion of cohorts from developing nations limit the usefulness of the data for physicians and parents dealing with EPIs in developed nations.

The above 2 studies58,59 confirm the need for our methodologically robust and detailed examination of EPIs receiving contemporary neonatal care. We used the Meta-analysis of Observational Studies in Epidemiology checklist24 to minimize the risk with pooling diverse observational data56 and obtain accurate, generalizable, and less biased results. We made extensive efforts to contact investigators. Multiple raters, blinded to each others’ assessments, examined each title, abstract, and full-text article. We set stringent inclusion criteria. Cohorts required 65% or more follow-up of survivors, as we sought to minimize biased NDI estimations resulting from an excessive attrition rate.6063 We selected follow-up assessments at 4 to 8 years because of the lower NDI rates when compared with follow-up at 18 to 36 months2123; results56,57,59 from early outcomes must be interpreted with caution.14 Prospective data collection removed the hazards of retrospective data. Choosing validated neurodevelopmental assessment methods36,64 and clear definitions of moderate and severe NDI enhances the quality of our data and ensures that our results have greater meaning to the medical community.

The significant decrease in moderate to severe NDI rates between each successive EPI week of gestation (Figure 3) may seem obvious and easily attributable to a rise in GA, but it goes against a recent argument65 used to support the notion of gestational ageism.66 Meadow and his coauthors65 used survival and NDI rates for EPIs from the United States,67 Great Britain,37 and France68 to demonstrate that the neurodevelopmental outcomes between each EPI week of gestation did not differ significantly. We believe that our data provide a more realistic and statistically stronger picture supported by low heterogeneity between study estimates; the decrease in NDI rates may be of clinical importance to some parents and physicians and should not be disregarded. We are unable to state that an increase in GA is the sole factor resulting in improved NDI rates because various possible confounders6,56,67,69 (eg, antenatal use of corticosteroids and parents’ socioeconomic status) can affect the rate of NDI. For severe NDI rates, there was a nonsignificant decrease with successive weeks of GA. This may be the result of a more limited sample size16 or support the argument of Meadow et al65 and a similar one by Andrews et al.6

There are limitations to our data and methods. First, we assessed only studies published in English. The likelihood of finding any non-English high-quality data on our subject matter appears minimal,58,70 particularly given our focus on developed nations and the global representation of cohorts included. Second, we did not report on survival rates to allow for an assessment of their relationship to the NDI rates.57 Although this assessment could examine a potential selection bias against sicker infants (ie, lower NDI rates in cohorts with lower survival rates), reports of survival rates are fraught with their own biases,13 thus bringing the usefulness of this assessment into question. Third, the lack of a term-control group in some cohorts presents a potential problem because the mean values on standardized developmental tests may be different than the expected normative mean depending on the specific term population. The result can be an underestimation of NDI.71,72 A term-control group also allows for blinding of those assessing for NDI, thereby enhancing the validity of the data. We performed a simple comparison of NDI rates in cohorts with a term-control group vs those without. These moderate to severe NDI rates did not differ significantly except at 24 weeks’ GA; however, this finding did not remain significant after adjustment for multiple comparisons. This provides some reassurance that our results do not underestimate the rate of NDI. Fourth, our inclusion of a cohort (EPIPAGE50) with a follow-up rate of less than 70% raises the concern of introducing bias despite 8 of the 9 cohorts having follow-up rates of more than 75%. A reanalysis of the data excluding EPIPAGE showed no notable differences (data not shown), reassuring us that our results remain valid.

Four points must be noted when contemplating the clinical use of our data. First, the high heterogeneity scores and wide confidence intervals around some of the results prevent clinicians from being able to give parents precise predictions. The high heterogeneity scores likely reflect differences in practice in the globally represented regions in our analysis,73 and the wide confidence intervals mostly reflect the small sample sizes at the lowest GA. These realities of the present data lend support to the use of high-quality local data when available and accentuate the need for further examination of why the NDI rates of EPIs are better in some regions of the world than others.

Second, the contribution of each cohort to the data differs. At 22 weeks’ GA, one cohort55 composed nearly half of the sample size and thus limits generalizability because single-center reports have inherent biases in their EPI population and management.15 For the other GA weeks, EPICure37 is the largest contributor but the other cohorts representing various regions of the developed world contribute to nearly the same degree, suggesting that our results are generalizable to many centers, although they may underestimate the NDI rates in comparison with smaller, less academic centers.

Third, although we selected frequently used definitions of NDI that affect children and families,40,41 we know that the perceptions of the effect of NDI on quality of life vary greatly.12,74,75 In the end, it is the perception of those living with the NDI that should matter the most.

Finally, clinicians may not be aware of the multiple limitations of published outcomes for EPIs. Even when using the best available data, clinicians need to be aware of and acknowledge these limitations to have clear and informed discussions with expectant parents when making shared decisions about an individual EPI’s care plan in the face of uncertainty.12,20,67,7476 In our opinion, this meta-analysis will assist clinicians or organizations in generating care plans, guidelines, or policies around EPI management but should not be used in isolation to enforce specific care plans at any particular GA.

In conclusion, our results provide the highest-quality pooled data to date on the NDI rates of EPI survivors. Knowledge of our results along with their limitations should aid physicians and parents in the SDM process regarding the care plan for an EPI. Given the relatively low number of high-quality cohorts in the literature, new antenatally recruited, prospective, and complete cohorts are warranted.

Accepted for Publication: February 24, 2013.

Corresponding Author: Gregory P. Moore, MD, FRCPC, Division of Newborn Care, The Ottawa Hospital, General Campus, Box 806, 501 Smyth Rd, Ottawa, ON K1H 8L6, Canada (gmoore@cheo.on.ca).

Published Online: August 26, 2013. doi:10.1001/jamapediatrics.2013.2395.

Author Contributions:Study concept and design: Moore, Lemyre, Daboval.

Acquisition of data: Moore, Lemyre, Daboval.

Analysis and interpretation of data: All authors.

Drafting of the manuscript: Moore.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Moore, Barrowman.

Administrative, technical, and material support: Moore.

Study supervision: Moore.

Conflict of Interest Disclosures: None reported.

Additional Contributions: Margaret Sampson, MLIS, PhD, AHIP, Childrens Hospital of Eastern Ontario, developed the search strategy, and Ruth Foxlee, Grad Dip Library & Information Science, MSc, Cochrane Wounds Group, Department of Health Sciences, University of York, peer reviewed the MEDLINE search strategy. Lex Doyle, MD, PhD, The Royal Women’s Hospital and University of Melbourne, provided input on our methodology. Thierry Lacaze, MD, PhD, and Samantha Somers, BA, Children’s Hospital of Eastern Ontario, critically reviewed the manuscript. The following individuals and groups shared additional data to facilitate this meta-analysis: Nele Stahlmann, MD, Blanka Zlatohlavkova, MD, the Extremely Low Birth Weight Infants in Finland Study group, the Norwegian Extreme Prematurity group, the EPIPAGE Study group, the Victorian Infant Collaborative Study group, and the Canterbury Child Development Research Group.

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Melchers  P, Preuss  U.  Adaptation of the Kaufman Assessment Battery for Children for German-speaking areas, part 1: introduction of the battery [in German]. Z Kinder Jugendpsychiatr. 1992;20(2):85-93.
PubMed
Palisano  R, Rosenbaum  P, Walter  S, Russell  D, Wood  E, Galuppi  B.  Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-223.
PubMed   |  Link to Article
Marlow  N, Wolke  D, Bracewell  MA, Samara  M; EPICure Study Group.  Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med. 2005;352(1):9-19.
PubMed   |  Link to Article
Roberts  G, Anderson  PJ, De Luca  C, Doyle  LW; Victorian Infant Collaborative Study Group.  Changes in neurodevelopmental outcome at age eight in geographic cohorts of children born at 22-27 weeks’ gestational age during the 1990s. Arch Dis Child Fetal Neonatal Ed. 2010;95(2):F90-F94.
PubMed   |  Link to Article
Mikkola  K, Ritari  N, Tommiska  V,  et al.  Neurodevelopmental outcome at 5 years of age of a national cohort of extremely low birth weight infants who were born in 1996-1997. Pediatrics. 2005;116(6):1391-1400.
PubMed   |  Link to Article
Drotar  D, Hack  M, Taylor  G, Schluchter  M, Andreias  L, Klein  N.  The impact of extremely low birth weight on the families of school-aged children. Pediatrics. 2006;117(6):2006-2013.
PubMed   |  Link to Article
Stephens  BE, Bann  CM, Poole  WK, Vohr  BR.  Neurodevelopmental impairment: predictors of its impact on the families of extremely low birth weight infants at 18 months. Infant Ment Health J. 2008;29(6):570-587.
PubMed   |  Link to Article
DerSimonian  R, Laird  N.  Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177-188.
PubMed   |  Link to Article
Higgins  JP, Thompson  SG.  Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539-1558.
PubMed   |  Link to Article
Holm  S.  A simple sequentially rejective multiple test procedure. Scand J Stat Theory Applications. 1979;6(2):65-70.
Wacholder  S.  Binomial regression in GLIM: estimating risk ratios and risk differences. Am J Epidemiol. 1986;123(1):174-184.
PubMed
Deddens  JA, Petersen  MR.  Approaches for estimating prevalence ratios. Occup Environ Med. 2008;65(7):481, 501-506.
Link to Article
R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
Schwarzer G. meta: meta-analysis with R: Updated: 11-29-2012. http://CRAN.R-project.org/package=meta. Accessed July 16, 2013.
Moher  D, Liberati  A, Tetzlaff  J, Altman  DG; PRISMA Group.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339(7716):b2535. doi:10.1136/bmj.b2535.
PubMed   |  Link to Article
Larroque  B, Ancel  PY, Marret  S,  et al; EPIPAGE Study group.  Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet. 2008;371(9615):813-820.
PubMed   |  Link to Article
Leversen  KT, Sommerfelt  K, Rønnestad  A,  et al.  Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm. Pediatrics. 2011;127(3):e630-e638. doi:10.1542/peds.2010-1001.
PubMed   |  Link to Article
Stahlmann  N, Rapp  M, Herting  E, Thyen  U.  Outcome of extremely premature infants at early school age: health-related quality of life and neurosensory, cognitive, and behavioral outcomes in a population-based sample in northern Germany. Neuropediatrics. 2009;40(3):112-119.
PubMed   |  Link to Article
Steinmacher  J, Pohlandt  F, Bode  H, Sander  S, Kron  M, Franz  AR.  Neurodevelopmental follow-up of very preterm infants after proactive treatment at a gestational age of ≥23 weeks. J Pediatr. 2008;152(6):771-776, e1-e2. doi:10.1016/j.jpeds.2007.11.004.
PubMed   |  Link to Article
Woodward  LJ, Moor  S, Hood  KM,  et al.  Very preterm children show impairments across multiple neurodevelopmental domains by age 4 years. Arch Dis Child Fetal Neonatal Ed. 2009;94(5):F339-F344. doi:10.1136/adc.2008.146282.
PubMed   |  Link to Article
Zlatohlávková  B, Kytnarová  J, Kuběna  A, Fleischnerová  A, Dokoupilová  M, Plavka  R.  Five-year survival without major disability of extremely preterm infants born at 22-27 weeks’ gestation admitted to a NICU. Acta Paediatr. 2010;99(11):1618-1623.
PubMed   |  Link to Article
Baron  IS, Rey-Casserly  C.  Extremely preterm birth outcome: a review of four decades of cognitive research. Neuropsychol Rev. 2010;20(4):430-452.
PubMed   |  Link to Article
Lorenz  JM.  Survival and long-term neurodevelopmental outcome of the extremely preterm infant: a systematic review. Saudi Med J. 2011;32(9):885-894.
PubMed
Bhutta  AT, Cleves  MA, Casey  PH, Cradock  MM, Anand  KJ.  Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA. 2002;288(6):728-737.
PubMed   |  Link to Article
Mwaniki  MK, Atieno  M, Lawn  JE, Newton  CR.  Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet. 2012;379(9814):445-452.
PubMed   |  Link to Article
Ganz  ML, Tendulkar  SA.  Mental health care services for children with special health care needs and their family members: prevalence and correlates of unmet needs. Pediatrics. 2006;117(6):2138-2148.
PubMed   |  Link to Article
Castro  L, Yolton  K, Haberman  B,  et al.  Bias in reported neurodevelopmental outcomes among extremely low birth weight survivors. Pediatrics. 2004;114(2):404-410.
PubMed   |  Link to Article
Wariyar  UK, Richmond  S.  Morbidity and preterm delivery: importance of 100% follow-up. Lancet. 1989;1(8634):387-388.
PubMed   |  Link to Article
Wolke  D, Söhne  B, Ohrt  B, Riegel  K.  Follow-up of preterm children: important to document dropouts. Lancet. 1995;345(8947):447.
PubMed   |  Link to Article
Tager-Flusberg  H, Plesa-Skwerer  D. Assessment of intelligence. In: Carey  WB, Crocker  AC, Elias  ER, Feldman  HM, Coleman  WL, eds. Developmental-Behavioural Pediatrics. Philadelphia, PA: Elsevier; 2009:811-827.
Meadow  W, Lagatta  J, Andrews  B, Lantos  J.  The mathematics of morality for neonatal resuscitation. Clin Perinatol. 2012;39(4):941-956.
PubMed   |  Link to Article
Wilkinson  DJ.  Gestational ageism. Arch Pediatr Adolesc Med. 2012;166(6):567-572.
PubMed
Tyson  JE, Parikh  NA, Langer  J, Green  C, Higgins  RD; National Institute of Child Health and Human Development Neonatal Research Network.  Intensive care for extreme prematurity—moving beyond gestational age. N Engl J Med. 2008;358(16):1672-1681.
PubMed   |  Link to Article
Larroque  B, Ancel  PY, Marchand-Martin  L,  et al; Epipage Study Group.  Special care and school difficulties in 8-year-old very preterm children: the Epipage cohort study. PLoS One. 2011;6(7):e21361. doi:10.1371/journal.pone.0021361.
PubMed   |  Link to Article
Leversen  KT, Sommerfelt  K, Rønnestad  A,  et al.  Predicting neurosensory disabilities at two years of age in a national cohort of extremely premature infants. Early Hum Dev. 2010;86(9):581-586.
PubMed   |  Link to Article
Grégoire  G, Derderian  F, Le Lorier  J.  Selecting the language of the publications included in a meta-analysis: is there a Tower of Babel bias? J Clin Epidemiol. 1995;48(1):159-163.
PubMed   |  Link to Article
Anderson  PJ, De Luca  CR, Hutchinson  E, Roberts  G, Doyle  LW; Victorian Infant Collaborative Group.  Underestimation of developmental delay by the new Bayley-III Scale. Arch Pediatr Adolesc Med. 2010;164(4):352-356.
PubMed   |  Link to Article
Wolke  D, Ratschinski  G, Ohrt  B, Riegel  K.  The cognitive outcome of very preterm infants may be poorer than often reported: an empirical investigation of how methodological issues make a big difference. Eur J Pediatr. 1994;153(12):906-915.
PubMed   |  Link to Article
Bodeau-Livinec  F, Marlow  N, Ancel  PY, Kurinczuk  JJ, Costeloe  K, Kaminski  M.  Impact of intensive care practices on short-term and long-term outcomes for extremely preterm infants: comparison between the British Isles and France. Pediatrics. 2008;122(5):e1014-e1021. doi:10.1542/peds.2007-2976.
PubMed   |  Link to Article
Saigal  S, Stoskopf  BL, Feeny  D,  et al.  Differences in preferences for neonatal outcomes among health care professionals, parents, and adolescents. JAMA. 1999;281(21):1991-1997.
PubMed   |  Link to Article
Saigal  S, Stoskopf  B, Pinelli  J,  et al.  Self-perceived health-related quality of life of former extremely low birth weight infants at young adulthood. Pediatrics. 2006;118(3):1140-1148.
PubMed   |  Link to Article
Pignotti  MS, Donzelli  G.  Perinatal care at the threshold of viability: an international comparison of practical guidelines for the treatment of extremely preterm births. Pediatrics. 2008;121(1):e193-e198. doi:10.1542/peds.2007-0513.
PubMed   |  Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.
Flow of Information Through Systematic Review

The Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines were used for selection and screening of data.49

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.
Random-Effects Meta-analysis of Moderate to Severe and Severe Neurodevelopmental Impairment Rates

Data markers indicate mean value; whiskers, 95% CI; and diamonds, pooled estimate (width of the diamond represents the 95% CI).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.
Random-Effects Meta-analysis of the Risk Difference of Neurodevelopmental Impairment for Each Additional Week of Gestational Age (GA)

Data markers indicate mean value; whiskers, 95% CI; and diamonds, pooled estimate (width of the diamond represents the 95% CI).

Graphic Jump Location

Tables

Table Graphic Jump LocationTable.  Description of Included Studies Including Assessment of Study Quality

References

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Hack  M, Taylor  HG, Drotar  D,  et al.  Poor predictive validity of the Bayley Scales of Infant Development for cognitive function of extremely low birth weight children at school age. Pediatrics. 2005;116(2):333-341.
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Wechsler  D. Wechsler Preschool and Primary Scale of Intelligence—Revised. San Antonio, TX: Psychological Corp; 1989.
Terman  LM, Merrill  MA. Stanford-Binet Intelligence Scale: Manual for the Third Revision Form L-M 1972 Norm. Boston, MA: Houghton Mifflin; 1973.
Melchers  P, Preuss  U.  Adaptation of the Kaufman Assessment Battery for Children for German-speaking areas, part 1: introduction of the battery [in German]. Z Kinder Jugendpsychiatr. 1992;20(2):85-93.
PubMed
Palisano  R, Rosenbaum  P, Walter  S, Russell  D, Wood  E, Galuppi  B.  Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-223.
PubMed   |  Link to Article
Marlow  N, Wolke  D, Bracewell  MA, Samara  M; EPICure Study Group.  Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med. 2005;352(1):9-19.
PubMed   |  Link to Article
Roberts  G, Anderson  PJ, De Luca  C, Doyle  LW; Victorian Infant Collaborative Study Group.  Changes in neurodevelopmental outcome at age eight in geographic cohorts of children born at 22-27 weeks’ gestational age during the 1990s. Arch Dis Child Fetal Neonatal Ed. 2010;95(2):F90-F94.
PubMed   |  Link to Article
Mikkola  K, Ritari  N, Tommiska  V,  et al.  Neurodevelopmental outcome at 5 years of age of a national cohort of extremely low birth weight infants who were born in 1996-1997. Pediatrics. 2005;116(6):1391-1400.
PubMed   |  Link to Article
Drotar  D, Hack  M, Taylor  G, Schluchter  M, Andreias  L, Klein  N.  The impact of extremely low birth weight on the families of school-aged children. Pediatrics. 2006;117(6):2006-2013.
PubMed   |  Link to Article
Stephens  BE, Bann  CM, Poole  WK, Vohr  BR.  Neurodevelopmental impairment: predictors of its impact on the families of extremely low birth weight infants at 18 months. Infant Ment Health J. 2008;29(6):570-587.
PubMed   |  Link to Article
DerSimonian  R, Laird  N.  Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177-188.
PubMed   |  Link to Article
Higgins  JP, Thompson  SG.  Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539-1558.
PubMed   |  Link to Article
Holm  S.  A simple sequentially rejective multiple test procedure. Scand J Stat Theory Applications. 1979;6(2):65-70.
Wacholder  S.  Binomial regression in GLIM: estimating risk ratios and risk differences. Am J Epidemiol. 1986;123(1):174-184.
PubMed
Deddens  JA, Petersen  MR.  Approaches for estimating prevalence ratios. Occup Environ Med. 2008;65(7):481, 501-506.
Link to Article
R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
Schwarzer G. meta: meta-analysis with R: Updated: 11-29-2012. http://CRAN.R-project.org/package=meta. Accessed July 16, 2013.
Moher  D, Liberati  A, Tetzlaff  J, Altman  DG; PRISMA Group.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339(7716):b2535. doi:10.1136/bmj.b2535.
PubMed   |  Link to Article
Larroque  B, Ancel  PY, Marret  S,  et al; EPIPAGE Study group.  Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet. 2008;371(9615):813-820.
PubMed   |  Link to Article
Leversen  KT, Sommerfelt  K, Rønnestad  A,  et al.  Prediction of neurodevelopmental and sensory outcome at 5 years in Norwegian children born extremely preterm. Pediatrics. 2011;127(3):e630-e638. doi:10.1542/peds.2010-1001.
PubMed   |  Link to Article
Stahlmann  N, Rapp  M, Herting  E, Thyen  U.  Outcome of extremely premature infants at early school age: health-related quality of life and neurosensory, cognitive, and behavioral outcomes in a population-based sample in northern Germany. Neuropediatrics. 2009;40(3):112-119.
PubMed   |  Link to Article
Steinmacher  J, Pohlandt  F, Bode  H, Sander  S, Kron  M, Franz  AR.  Neurodevelopmental follow-up of very preterm infants after proactive treatment at a gestational age of ≥23 weeks. J Pediatr. 2008;152(6):771-776, e1-e2. doi:10.1016/j.jpeds.2007.11.004.
PubMed   |  Link to Article
Woodward  LJ, Moor  S, Hood  KM,  et al.  Very preterm children show impairments across multiple neurodevelopmental domains by age 4 years. Arch Dis Child Fetal Neonatal Ed. 2009;94(5):F339-F344. doi:10.1136/adc.2008.146282.
PubMed   |  Link to Article
Zlatohlávková  B, Kytnarová  J, Kuběna  A, Fleischnerová  A, Dokoupilová  M, Plavka  R.  Five-year survival without major disability of extremely preterm infants born at 22-27 weeks’ gestation admitted to a NICU. Acta Paediatr. 2010;99(11):1618-1623.
PubMed   |  Link to Article
Baron  IS, Rey-Casserly  C.  Extremely preterm birth outcome: a review of four decades of cognitive research. Neuropsychol Rev. 2010;20(4):430-452.
PubMed   |  Link to Article
Lorenz  JM.  Survival and long-term neurodevelopmental outcome of the extremely preterm infant: a systematic review. Saudi Med J. 2011;32(9):885-894.
PubMed
Bhutta  AT, Cleves  MA, Casey  PH, Cradock  MM, Anand  KJ.  Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA. 2002;288(6):728-737.
PubMed   |  Link to Article
Mwaniki  MK, Atieno  M, Lawn  JE, Newton  CR.  Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet. 2012;379(9814):445-452.
PubMed   |  Link to Article
Ganz  ML, Tendulkar  SA.  Mental health care services for children with special health care needs and their family members: prevalence and correlates of unmet needs. Pediatrics. 2006;117(6):2138-2148.
PubMed   |  Link to Article
Castro  L, Yolton  K, Haberman  B,  et al.  Bias in reported neurodevelopmental outcomes among extremely low birth weight survivors. Pediatrics. 2004;114(2):404-410.
PubMed   |  Link to Article
Wariyar  UK, Richmond  S.  Morbidity and preterm delivery: importance of 100% follow-up. Lancet. 1989;1(8634):387-388.
PubMed   |  Link to Article
Wolke  D, Söhne  B, Ohrt  B, Riegel  K.  Follow-up of preterm children: important to document dropouts. Lancet. 1995;345(8947):447.
PubMed   |  Link to Article
Tager-Flusberg  H, Plesa-Skwerer  D. Assessment of intelligence. In: Carey  WB, Crocker  AC, Elias  ER, Feldman  HM, Coleman  WL, eds. Developmental-Behavioural Pediatrics. Philadelphia, PA: Elsevier; 2009:811-827.
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PubMed   |  Link to Article
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