PEDIATRICS Vol. 123 No. 2 February 2009, pp. 723-730 (doi:10.1542/peds.2007-2564)
ARTICLE |
Can Birth Weight Standards Based on Healthy Populations Improve the Identification of Small-for-Gestational-Age Newborns at Risk of Adverse Neonatal Outcomes?
a Centre d'Epidémiologie des Populations EA4184, Université de Bourgogne, Dijon, France
b Cellule d'Évaluation du Réseau Périnatal de Bourgogne
d Service de Biostatistiques et d'Informatique Médicale
h Service de Pédiatrie
g Service d'Obstétrique, CHRU Dijon, France
c INSERM, U866
f Centre d'Investigation Clinique-Epidémiologie Clinique/Essais Cliniques CIE1, Dijon, France
e Department of Epidemiology and Biostatistics, McGill University, Montreal, Quebec, Canada
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ABSTRACT |
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 TOP ABSTRACT PATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVES. To develop neonatal growth standards based on (1) the entire population of live births and (2) a healthy subpopulation and compare them in identifying infants as small for gestational age and at risk of adverse neonatal outcomes.
PATIENTS AND METHODS. We included all births, between 28 and 41 weeks of gestation, reported in Burgundy (France) from 2000 to 2006. Fetal deaths, multiple births, and chromosomal aberrations were excluded. We first estimated separate birth weight distributions at each week of gestation for (1) all neonates and (2) only infants born from women without maternal diseases. Small for gestational age was defined as a birth weight below the 10th percentile of the corresponding standard. We assessed the associations of small for gestational age on the basis of the alternative definitions, with mortality and major neonatal outcomes.
RESULTS. We included 127 584 live births. For term newborns, small for gestational age was significantly associated with an increased risk of death with both standards. In contrast, for preterm newborns (32–36 weeks), small for gestational age was not significantly associated with mortality and morbidity. Very preterm infants (28–31 weeks) identified as small for gestational age according to the healthy-population standard were at higher risk of chronic lung disease and intraventricular hemorrhage. When using the entire-population standard, small for gestational age was associated with chronic lung disease but not intraventricular hemorrhage. The area under the receiver operating characteristic for predicting an intraventricular hemorrhage was significantly greater for small for gestational age defined with the healthy-population standard compared with small for gestational age classified with the entire-population standard.
CONCLUSIONS. Neonatal growth standards based on healthy populations could improve the identification of very preterm neonates as small for gestational age and at risk of intraventricular hemorrhage.
Key Words: birth weight • growth standard • small for gestational age • intrauterine growth restriction • adverse neonatal outcome • intraventricular hemorrhage • sepsis
Abbreviations: IUGR—intrauterine growth restriction • BW—birth weight • GA—gestational age • SGA—small for gestational age • RDS—respiratory distress syndrome • IVH—intraventricular hemorrhage • c-PVL—cystic periventricular leukomalacia • CLD—chronic lung disease • HIE—hypoxic-ischemic encephalopathy • OR—odds ratio • CI—confidence interval • ROC—receiver operating characteristic • AUC—area under the curve • AGA—appropriate for gestational age
Intrauterine growth restriction (IUGR) is defined as reduced growth during fetal life relative to the genetic potential of the fetus. Infants with IUGR at birth are usually identified by comparing their birth weight (BW) to a distribution of weights corresponding to the same gestational age (GA) in a population considered as a reference. On the basis of such comparisons, newborns may be classified as small for gestational age (SGA), a proxy for IUGR. In several studies, IUGR has been shown to be associated with increased mortality and morbidity in newborn infants.1,2 However, the relationships between SGA and mortality or morbidity may depend on the reference used.3–5 Indeed, published weight growth references were established by using different populations and methods, and there is no consensus regarding the "optimal" reference.5–8 Moreover, authors of various studies5,8–10 have recommended the use of fetal growth standards rather than neonatal standards estimated from live birth infants only to improve the identification of preterm infants as SGA and at risk of adverse outcomes.
Furthermore, many preterm and very preterm deliveries are associated with maternal diseases (especially hypertension) that affect the weight of fetuses.11,12 Thus, neonatal BW standards defined on populations, which include these diseases, may not adequately represent the natural intrauterine growth trajectory of healthy fetuses.10,13 We can assume that a proxy of normal fetal weight could be obtained from BWs of a population free of maternal diseases that may impact the weight of fetuses. To our knowledge, no authors have performed a study that compared the relative risks of adverse outcomes associated with an SGA classification based on a BW reference derived from the entire population versus an SGA classification based on a healthy population free of maternal diseases. Therefore, our aims for this study were to construct 2 gender- and GA-specific BW standards, 1 based on the entire population of live births and another obtained on a healthy population from which infants with relevant maternal diseases were excluded, and then to compare the ability of the 2 standards to identify infants with poor neonatal prognosis.
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PATIENTS AND METHODS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Since 2000, all births that occur in Burgundy at or after 22 completed weeks of gestation and/or with a BW of >500 g, are systematically recorded in an anonymous database used to regularly assess the Burgundy perinatal network procedures.14 This database contains the data of >99.9% of all births in the region.14 Information about clinical events is collected prospectively for mothers and newborns between birth and hospital discharge. This information includes individual perinatal data such as maternal diseases, pregnancy outcome, BW, GA, infant gender, newborns with diseases, and outcomes. The GA, in completed weeks of gestation, is assessed on the basis of the mother's last menstrual period and confirmed or modified, when necessary, by routine an early antenatal ultrasound scan that is performed, in France, for
95% of pregnant women.15 Standardized definitions of diseases, guidelines for coding, validation of data, and completeness of the database are regularly ensured.14 We included in this study all births of infants between 28 and 41 weeks of gestation, born in Burgundy between January 2000 and December 2006. Fetal deaths, multiple births, chromosomal aberrations, and infants with missing BW or gender data were excluded. Infants with implausible BW for their GA were identified through a normal mixture model, which estimates the probability of an infant having an inaccurate GA on the basis of the GA-specific BW distributions in the entire database.16 All infants with the estimated probability of incorrect GA above 0.95 were considered to have an implausible BW for their GA and were excluded.
After these exclusions, we estimated BW distributions for each week of GA, separately for boys and girls, and verified their normality with Kolmogorov-Smirnoff and Shapiro-Wilks tests. We first estimated distributions by using all infants of a given gender and born at a given GA to obtain standards based on the entire population ("BurgundyE"). Then, we estimated distributions after having excluded births from mothers with maternal diseases known to impact the BW (diabetes, maternal hypertension, preeclampsia, eclampsia, abruptio placentae, placenta previa, presumed chorioamnionitis) to obtain a "healthy-population" standard ("BurgundyH"). Finally, for each of the 2 standards, we estimated selected percentiles (3rd, 10th, 50th, 90th, and 97th) of the gender-specific BW distributions at each GA week between 28 and 41. Similar to Kramer et al,17 these percentiles were estimated by a flexible generalized additive model,18 in which the corresponding empirical percentiles observed at consecutive weeks were smoothed by using smoothing splines with 4 degrees of freedom.19
Newborns were then classified as SGA separately according to the 10th percentile of the entire-population (SGABE) and healthy-population (SGABH) standards. The resulting SGA rates, at each GA, were compared by using the McNemar test for matched binary data.
We assessed associations between each SGA standard and each of the following major neonatal outcomes: respiratory distress syndrome (RDS), intraventricular hemorrhage (IVH), cystic periventricular leukomalacia (c-PVL), and chronic lung disease (CLD) in preterm infants, hypoxic-ischemic encephalopathy (HIE) in term newborns, and in-hospital mortality in both preterm and term newborns. The diagnosis of IVH and c-PVL was assessed by using the same protocol for all very preterm infants (between 28 and 31 GA weeks): each infant had 2 sonographic screenings during the first week of life and every week until 40 weeks of postconceptional age. IVH was graded according to the Papile et al classification.20 c-PVL was diagnosed on the basis of the presence of echolucent areas or persistent echogenicity in periventricular areas on coronal and sagittal views of cranial ultrasounds.21 CLD was diagnosed in surviving neonates when the infant required oxygen supplementation beyond 36 weeks of postconceptional age. In Burgundy, the regional recommendations are to maintain an oxygen saturation between 93% and 95% at 36 weeks of postconceptional age. The diagnosis of RDS was established by a clinical assessor according to criteria proposed by Rubaltelli et al22: oxygen dependence increasing during the first 24 hours of life; exclusion of infection; typical radiologic pattern with reduced air content; and reticulonodular pattern of the lung and air bronchogram. In-hospital mortality was defined as a death occurring during the hospital stay.
Because the risk of an adverse outcome decreased sharply, in a nonlinear way, with increasing GA, we conducted separate analyses for each of the 3 GA strata, defined on the basis of clinical considerations: very preterm (28–31 weeks), preterm (32–36 weeks), and term neonates (
37 weeks). Within each stratum, we estimated the strength of the association between SGA, defined according to each standard, and the respective outcome by using multiple logistic regression, which adjusted for a continuous measure of GA and gender. First-order interactions between SGA and each of these 2 covariates were tested by a 2-tailed Wald test and excluded from the model if they did not reach statistical significance at the .05 level. Crude and adjusted odds ratios (ORs) for each SGA definition and their 95% confidence intervals (CIs) were estimated.
To further compare the 2 SGA classifications derived, respectively, from our entire population (SGABE) and from the healthy population (SGABH), we then estimated the 2 corresponding receiver operating characteristic (ROC) curves separately for each outcome. Each ROC curve was estimated by using the 3rd, 10th, and 50th percentiles as cutoffs, and the corresponding area under the curve (AUC) was calculated. The difference between the 2 AUC values were compared by using the test proposed by Hanley and McNeil.23,24
Statistical analyses were performed by using SAS 8.2 (SAS Institute, Inc, Cary, NC) and Stata 8.0 (Stata Corp, College Station, TX) packages. All hypotheses were tested at the 2-tailed .05 significance level.
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RESULTS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Between 2000 and 2006, 132 588 newborns from 28 to 41 GA weeks were identified in Burgundy. We excluded 11 infants (0.007%) with implausible BW for GA, 546 (0.41%) fetal deaths, 4141 (3.1%) multiple births, 215 (0.2%) infants with chromosomal aberrations, and 91 (0.07%) with missing BW or gender information. The "entire-population" BW distributions were estimated from the 127 584 (96.2%) remaining live births.
The "healthy-population" BW distributions were estimated from the 115 238 of these live births after the exclusion of 12 346 (9.7%) pregnancies with maternal diseases. The proportion of newborns excluded at each GA is reported in the last column of Tables 1 (male subjects) and 2 (female subjects). The rate of exclusions decreased linearly, from 60.8% at 28 weeks to 6.6% at 41 weeks (P < .0001). Maternal hypertension was the principal cause of exclusions: 31.8% in very preterm, 13.8% in preterm, and 3.5% in term newborns (P < .0001).
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The smoothed percentiles of BW, for each week of GA, for male and female subjects are reported, respectively, in Tables 1 and 2. As expected, because of the exclusion of the maternal diseases, for preterm infants the percentiles estimated from the healthy population (right half of each table: BurgundyH) are higher at each GA than the corresponding percentiles based on the entire population (left half of the table: BurgundyE). As the GA increased from 28 to 36 weeks, the differences in the 10th percentiles declined from 139 to 59 g for boys (Table 1) and from 282 to 53 g for girls (Table 2). Indeed, at 40 weeks the 2 standards agreed almost perfectly, with a difference of only 4 g for boys and 1 g for girls.
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Figure 1 compares the SGA rates estimated with the 2 standards for each week of GA. According to the entire-population standard, 11.0% of very preterm infants are classified as SGA. In contrast, as many as 30.4% of very preterm infants are classified as SGA, because they fall below the 10th percentile of the standard based on the healthy population (P < .0001). The rates of SGABE and SGABH are, respectively, 9.6% vs 13.6% for preterm infants (P < .0001) and 8.9% vs 9.2% for term newborns (P < .0001).
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Table 3 compares the frequency of the different neonatal outcomes in newborns identified as SGA on the basis of the entire population and in those identified on the basis of the healthy population, as well as among those classified as "appropriate" for their GA (AGA) according to the 2 standards. Among very preterm and term infants, the frequency of several outcomes was increased in the SGA subgroups. This increase did not occur for preterm infants.
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Table 4 describes the associations of SGABH and SGABE, with neonatal outcomes, separately for very preterm, preterm, and term newborns. For term newborns (
37 weeks), SGA is associated with a significantly increased risk of death, and as expected, the 2 standards show very similar associations (adjusted OR's: 3.8 for SGABH and 3.9 for SGABE). In contrast, for preterm newborns, SGA is not significantly associated with either outcome (Table 4). However, for very preterm newborns, regardless of the standard used, SGA is associated with a significantly increased risk of CLD (adjusted OR's: 3.0 for SGABH and 2.6 for SGABE).
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In very preterm newborns, the SGABH, defined on the basis of the healthy population, is associated with a significant increase in the risk of all grades of IVH (adjusted OR: 3.0 [95% CI: 1.9–5.0]; P < .0001). In contrast, the association with the SGABE, derived from the entire population, is completely nonsignificant (adjusted OR: 1.2 [95% CI: 0.6–2.6]; P = .56). Interestingly, we observed a similar nonsignificant trend when the analysis was limited to grades III/IV IVH (n = 11) with ORs of 2.8 (95% CI: 0.8–9.3; P = .09) for SGABH and 1.8 for SGABE (95% CI: 0.4–8.6; P = .44). The differences between the 2 associations remained similar even after adjustment for the use of antenatal steroids (data not shown). The sensitivity for predicting an all-grades IVH in very preterm infants was much higher for SGABH (53.2% [95% CI: 41.6–64.5]) compared with SGABE (11.4% [95% CI: 5.3–20.5]). The specificity was, respectively, 73.5% (95% CI: 69.3–77.3) versus 89.1% (95% CI: 86.0–91.7). Accordingly, the AUC under the ROC curve was significantly greater for BurgundyH (AUC: 0.678 [95% CI: 0.621–0.733]) than for BurgundyE (AUC: 0.573 [95% CI: 0.514–0.632]; P < .0001) (Fig 2). For other outcomes, no statistically significant differences between the ROC curves were found (data not shown). Yet, for all outcomes except c-PVL, in very preterm infants, SGABH showed stronger associations than SGABE (Table 4).
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When, for each morbidity outcome, we repeated similar analyses using the compound outcome of either a neonatal outcome or death, we found results similar to those presented in Table 4 (data not shown).
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DISCUSSION |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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In our study, very preterm newborns identified as SGA on the basis of the distributions of BW estimated from the healthy population had a threefold, statistically very significant, increase in the risk of IVH. In contrast, the SGA definition derived from the entire population, which included births affected by maternal diseases, was not associated with IVH. Accordingly, using the standard derived from the healthy population rather than from the entire population permitted a significant improvement in the identification of very preterm newborns at increased risk of IVH, as indicated by a significantly higher AUC under the ROC curve.
Our results were obtained from a large validated population database, the completeness and quality of which are regularly assessed.14 In particular, GA is systematically assessed by early ultrasound scan. These elements certainly contributed to the fact that we identified only an extremely low rate of infants with implausible BW for GA (<0.01%), although we relied on the state-of-the-art methodology to eliminate such outliers.16 Our database did not provide complete information on maternal smoking, and its prevalence (4.2%) was likely underestimated.15 Fitzgerald et al25 reported that the association between maternal smoking and SGA risk also varied with GA and became significant only after 32 weeks of gestation. Given these findings, our results for newborns between 28 and 31 weeks’ GA should not be materially affected by the incomplete information on maternal smoking. We checked, in a sensitivity analysis, that the exclusions of mothers known to have smoked during their pregnancy provided the same results (data not shown). Information about some other maternal diseases (thrombophilias, significant renal disease, and collagen vascular diseases) was not present in our database. We assumed that most of theses pathologies were excluded because of exclusion of maternal hypertension.
We found important differences between BW of the entire population and the healthy population, especially at low GA. The differences decreased with GA, because maternal diseases, excluded from the healthy population, were more prevalent among preterm newborns. These differences were similar to those reported in previous studies when comparing a fetal growth standard obtained from uncomplicated pregnancies against a neonatal growth standard obtained from the entire population.5,8 Accordingly, we found that the rates of SGA, based on the healthy population, were higher in preterm than in term newborns. As expected, the rates of SGA preterm newborns, classified with our healthy-population–based standard, were significantly higher than those obtained from the standard based on the entire population. Most importantly, the SGA rates based on the healthy-population standard were similar to those reported when using a fetal growth standard obtained from uncomplicated pregnancies.4,5,10 These findings are consistent with our hypothesis that BW distributions based on a population free of maternal diseases could approach the normal fetal weight.
In very preterm newborns, classified as SGA with our healthy-population standard, we found a marginally nonsignificant increase of the risk of death (P = .08). Previous studies4,5 revealed a similar increase of the risk of death in preterm SGA newborns classified with a fetal growth standard obtained from uncomplicated pregnancies. Our marginally nonsignificant result could be explained by a limited statistical power because of only 26 hospital neonatal deaths among very preterm newborns. Furthermore, several studies1,5,26–29 revealed an increase of the risk of death in SGA preterm newborns classified with a neonatal weight standard obtained from the entire population, especially below 28 weeks.26,28We did not observe this important increase of the risk of death in very preterm SGABE newborns. This may be because of exclusions of births below 28 weeks, which were too few to reliably estimate the percentiles of GA-specific BW distributions.
Our results suggested a marginally nonsignificantly reduced risk of RDS in preterm newborns classified as SGA, after adjustment for GA and gender (P = .06 for SGABE and P = .09 for SGABH), regardless of the standard used (Table 4). A similar protective effect was reported in previous studies.5,27 In contrast, some other studies revealed an increased risk of RDS in SGA preterm newborns.1,5,30 Ley et al4 found that SGA was associated with an increased risk of RDS in newborns below 29 weeks’ GA and a protective effect in newborns between 29 and 32 weeks’ GA, suggesting a relationship with preeclampsia. Additional investigation is required to clarify the relationship between preeclampsia, SGA, and RDS.
Furthermore, we found a statistically significant threefold increase of the risk of IVH, in very preterm neonates classified as SGA based on our healthy-population BW distribution, even after adjustment for GA and gender. In contrast, we found no statistically significant association when SGA was derived from entire-population, which included births affected by maternal diseases (Table 4). These findings are similar to previously reported findings of an association between SGA and IVH, based on a fetal standard, obtained from healthy mothers,5 but no association when neonatal standards, obtained from entire-populations, were used.5,11,27,29–33 IVH is a common cerebral morbidity whose frequency and seriousness are closely related to the degree of prematurity.34,35 We were able to demonstrate that SGABH was significantly more predictive of an IVH in very preterm newborns than SGABE, because the corresponding ROC curve had significantly higher AUC.
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CONCLUSIONS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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In this study, we found that using healthy-population BW standards was advantageous in very preterm infants, especially for the identification of newborns at risk of IVH. For these newborns, we found that neonatal BW standards based on healthy-populations gave similar results to those reported in studies that used fetal standards for the identification of IUGR at risk of adverse neonatal outcomes. However, the choice between healthy-population or entire-population BW standards did not affect the results of the analysis of IUGR for preterm and at term infants. Authors performing future studies should investigate the association between the causes of IUGR and adverse neonatal outcomes, and potential benefits of deriving SGA standards from different populations.
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ACKNOWLEDGMENTS |
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We thank the members of the Burgundy perinatal network and all physicians in hospitals of the Burgundy region (CH de Sens, Auxerre, Nevers, Dijon, Beaune, Chalon-sur-Saône, Mâcon, Montceau-les-Mines, Paray-le-Monial, Le Creusot, Semur en Auxois, Chatillon sur Seine, Autun, Decize, Clinique Sainte-Marthe, Clinique de Chenôve, Clinique d'Auxerre, and Clinique du Nohain).
Michal Abrahamowicz is a James McGill Professor of Biostatistics at McGill University.
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FOOTNOTES |
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Accepted Jun 3, 2008.
Address correspondence to Cyril Ferdynus, MS, Cellule d'Evaluation du Réseau Périnatal de Bourgogne, 1 Boulevard Jeanne d'Arc, B P-77908, 21079 Dijon Cedex, France. E-mail: cyril.ferdynus{at}chu-dijon.fr
The authors have indicated they have no financial relationships relevant to this article to disclose.
| What's Known on This Subject Neonatal BW standards defined on populations that include maternal diseases may be less appropriate for the identification of neonates as SGA and at risk of adverse outcome than fetal growth standards.
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| What This Study Adds The use of neonatal BW standards defined on healthy populations improves the identification of preterm neonates as SGA and at risk of poor neonatal outcome.
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PEDIATRICS (ISSN 1098-4275). ©2009 by the American Academy of Pediatrics
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