The Risks of Adverse Neonatal Outcome Among Preterm Small for Gestational Age Infants According to Neonatal Versus Fetal Growth Standards
* Department of Child Health, University of Aberdeen, Aberdeen, United Kingdom
Departments of Obstetrics and Gynecology
Paediatrics, St Joseph’s Health Care London, the University of Western Ontario, London, Ontario, Canada
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Objective. To evaluate neonatal and fetal growth standards in determining the impact of small for gestational age (SGA) on neonatal mortality and morbidity.
Design. A hospital-based cohort study of infants born in a regional tertiary care center and admitted to the neonatal intensive care unit.
Setting and Participants. A total of 1267 singleton neonates of <34 weeks gestational age, without any congenital anomalies, born between January 1, 1993 and December 31, 2001.
Outcome Measures. Each outcome variable including mortality, respiratory distress syndrome, bronchopulmonary dysplasia, intraventricular hemorrhage (IVH), periventricular leukomalacia, and necrotizing enterocolitis was related to growth status as defined by fetal and neonatal growth standards after adjustment for potential confounders.
Results. The number of SGA infants was 11.6% (n = 147) of the study population according to neonatal growth standards, but it was increased to 23.3% (n = 295) when fetal growth standards were used. According to fetal growth standards, when SGA was compared with appropriate for gestational age infants, it was associated with an increased risk of respiratory distress syndrome (odds ratio [OR] 1.40; 95% confidence interval [CI] 1.00–1.95), bronchopulmonary dysplasia (OR 2.18; 95% CI 1.33–3.59), IVH (OR 1.67; 95% CI 1.13–2.45), and retinopathy of prematurity (OR 3.88; 95% CI 2.33–6.48). However, only neonatal mortality (OR 3.64; 95% CI 1.64–8.09), retinopathy of prematurity (OR 5.38; 95% CI 2.87–10.90), and necrotizing enterocolitis (OR 2.47; 95% CI 1.21–5.07) were positively associated with SGA when using neonatal growth standards.
Conclusions. Compared with the neonatal growth standards, the fetal growth standards are better in identifying increased risk of respiratory morbidity and IVH among preterm SGA infants.
Key Words: neonatal outcome • small for gestational age
Abbreviations: SGA, small for gestational age • RDS, respiratory distress syndrome • AGA, appropriate for gestational age • AC, abdominal circumference • FL, femur length • IVH, intraventricular hemorrhage • BPD, bronchopulmonary dysplasia • NEC, necrotizing enterocolitis • ROP, retinopathy of prematurity • PVL, periventricular leukomalacia • OR, odds ratio • CI, confidence interval
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INTRODUCTION |
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Every year,
40 000 infants born at term in the United States are small for gestational age (SGA).1 SGA is associated with an increased risk of spontaneous and iatrogenic preterm delivery.2,3 Therefore, the impact of SGA on preterm infants cannot be underestimated. However, it is difficult to interpret the adverse effects of SGA on neonatal mortality and morbidity among preterm infants from the published data because SGA has been reported to be associated with either increased,4–6 decreased,7–9 or no change10 in incidence of respiratory distress syndrome (RDS). Similarly, the frequency of risk of intracranial hemorrhage and periventricular leucomalacia associated with SGA vary from one study to another.11 Ley et al12 have suggested that these different results may be partly influenced by the use of different diagnostic criteria and/or application of different growth standards. These investigators used intrauterine growth curves to demonstrate that SGA infants born before 29 weeks gestation are at increased risk of RDS. They found that fetal growth curves are more accurate than neonatal growth curves in identifying increased risk of RDS. Previously, it has been shown that the birth weight cutoff for specific percentiles varies depending on the growth standards used.13 There are differences in birth weight cutoff points between fetal and neonatal growth standards, and fetal growth standards are found to be more appropriate than neonatal growth standards in predicting the impact of size at birth on the risk of spontaneous preterm delivery.2
Because the fetal and the neonatal growth standards can possibly lead to different risk estimates for neonatal mortality and morbidity, the aim of this study was to determine which growth standard was more appropriate to identify adverse neonatal outcome among preterm SGA neonates when compared with appropriate for gestational age (AGA) neonates. We hypothesized that fetal growth standards are superior to neonatal growth standards in identifying preterm SGA neonates at risk of adverse outcomes.
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METHODS |
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This was a hospital-based cohort study of infants admitted to the Neonatal Intensive Care Unit between January 1, 1993 and December 31, 2001 at St Joseph’s Health Care London, London, Ontario, which is the perinatal tertiary care center in Southwestern Ontario, Canada. Details of infants were collected from their health records at the time of discharge, and stored in a computerized perinatal database. Data were entered after the death of an infant or after an infant was discharged from the hospital. From this database, infants who met the following criteria were included in the study: 1) singleton, 2) no congenital anomaly, 3) gestational age at birth <34 completed weeks, and 4) inborn.
The gestational age was recorded in completed weeks. It was estimated from the obstetric assessment by the first day of the last menstrual period, which was confirmed by early second trimester ultrasound. In cases of discordance of >10 days between last menstrual period and ultrasound derived gestational age, the ultrasound adjusted gestational age at delivery was used.
The neonates were classified as AGA or SGA according to their birth weight percentiles defined by fetal growth standards of Hadlock et al14 and neonatal growth standards of Arbuckle et al.15 Arbuckle’s neonatal growth standards were derived from birth weight data obtained from vital statistics and health department birth registrations for over 1 million live births in Canada from 1986–1988. These growth standards were corrected for gender. Hadlock et al14 developed fetal growth standards ultrasonographically from a population of middle-class white American patients with certain menstrual histories. The estimated fetal weight was calculated at the time of the ultrasound study by using a model based on measurements of biparietal diameter, head circumference, abdominal circumference (AC), and femur length (FL) in combination16 using the following formula: log10 weight = 1.3596 – 0.00386 AC x FL + 0.0064 head circumference + 0.00061 biparietal diameter x AC + 0.0424 AC + 0.174 FL.16
This population is similar to the predominantly white middle-class Canadian women with universal health coverage in Southwestern Ontario. Fetal growth standards are not corrected for gender as in utero sex determination may not be done accurately.
AGA infants were defined as those whose birth weights for gestational age were between the 10th and 90th percentiles (inclusive), and SGA infants were defined as those whose birth weights for gestational age fell below the 10th percentile.
RDS was diagnosed clinically (FIO2 >40% to maintain a PaO2 >50 torr in the absence of clinical evidence of pneumonia, sepsis, or other causes of respiratory distress)5 and radiologically.17 Bronchopulmonary dysplasia (BPD) was diagnosed when the infant required oxygen supplemention beyond 28 days of postnatal age and showed abnormal radiologic evidence.18 The extent of intraventricular hemorrhage (IVH) was graded according to the classification by Papile et al19 and necrotizing enterocolitis (NEC) was staged according to Bell’s classification.20 Retinopathy of prematurity (ROP) was classified according to international classification ranging from stage 1 to 5.21 Periventricular leukomalacia (PVL) was diagnosed by echolucent areas or persistent echogenicity in periventricular areas on coronal and sagittal views of cranial ultrasounds.22
Statistics
For each outcome variable (mortality, RDS, BPD, assisted ventilation, IVH, PVL, ROP, and NEC), separate analyses were performed comparing SGA and AGA infants classified by either neonatal or fetal growth standards. Multiple logistic regression analysis adjusted for use of antenatal steroids and gender were performed to relate each outcome variable to growth status (SGA or AGA). A variable was considered to be significantly associated with outcome if the odds ratio (OR) differed from 1.0 and the P value was <.05. Statistical analysis was performed using SAS version 6.12 (SAS Institute, Cary, North Carolina).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Characteristics of the Study Population
During the study period, 1267 infants born at <34 weeks gestation were admitted to the center. There were 712 (56.2%) male infants and 555 (43.8%) female infants. These infants were stratified as SGA and AGA according to birth weight percentiles by the fetal growth standards of Hadlock et al14 and the neonatal growth standards of Arbuckle et al.15
The birth weight cutoff points for the 10th and 90th percentiles between the fetal growth standards of Hadlock et al14 and the neonatal growth standards of Arbuckle et al15 have been reported elsewhere.2 The birth weight difference between fetal and neonatal growth standards varied from 32 g to 203 g for males and from 52 g to 273 g for females among the preterm infants of 25 to 34 weeks gestation at the 10th percentile. According to the neonatal growth standard, 147 (11.6%) of the study population weighed less than the 10th percentile at birth and 852 (67.2%) weighed between the 10th and 90th percentile. However, infants of birth weights of less than the 10th percentile and of 10th and 90th percentiles were 295 (23.3%) and 857 (67.6%), respectively, when the fetal growth standard was applied. The incidence of the different outcome variables studied using neonatal or fetal growth standards are shown in Table 1.
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Neonatal Mortality
Multiple logistic regression analysis was conducted with adjustments for sex and use of antenatal steroids, and ORs and 95% confidence interval (CI) were calculated to determine the effect of SGA according to fetal and neonatal growth standards on neonatal mortality and morbidity (Table 2). The AGA group was used as the reference for the study population. There was a 3.6-fold greater risk of neonatal mortality in preterm SGA infants as compared with AGA infants according to the neonatal growth standards. In contrast, when using the fetal growth standards, SGA was not associated with an increased risk of neonatal mortality when compared with the AGA group (Table 2).
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Neonatal Morbidity
Table 1 shows the effects of neonatal or fetal growth standards on the incidence of different variables of neonatal morbidity including RDS, assisted ventilation, BPD, IVH, PVL, NEC, and ROP. Adjusted ORs with 95% CI comparing neonatal morbidity between SGA and AGA groups using each growth standard are illustrated in Table 2.
When using fetal growth standards, the risk of RDS, need for assisted ventilation, BPD, IVH, and ROP among the preterm SGA infants were high. There was a trend for increased risk of NEC among this population, although it did not reach statistical significance. In contrast, when using neonatal growth standards, only the risk of ROP and NEC were increased in preterm SGA infants when compared with the AGA group. There was no statistically significant difference in the risk of RDS, assisted ventilation, BPD, or IVH.
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DISCUSSION |
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Previous studies have shown that SGA is more common in preterm than in term infants.3,23–25 Our study has demonstrated that a small size at birth, in preterm infants consisting of birth weights less than the 10th percentile for gestational age classified according to the fetal growth standards, is associated with a significantly increased risk of neonatal respiratory morbidity and IVH. In contrast, the use of neonatal growth standards to identify SGA as an independent risk factor did not demonstrate an increased risk of neonatal respiratory morbidity including RDS, need for assisted ventilation and BPD, or IVH. Furthermore, fetal growth standards identified a 2-fold greater proportion of neonates as SGA when compared with neonatal growth standards in preterm infants <34 weeks gestation.
Piper et al10 showed that the neonatal mortality of infants with a birth weight of less than the 10th percentile was higher than in AGA neonates at each gestational age up to 36 weeks. Bernstein et al6 also found an increased risk in neonatal death in SGA neonates from 25 to 30 weeks gestation. In both studies, neonatal growth standards were used. Similarly, we have observed a 3.6-fold increase of mortality in preterm neonates classified as SGA using neonatal growth standards. When using fetal growth standards, we observed a nonsignificant higher risk of mortality in SGA neonates (OR: 1.62). A larger population-based study from Ley et al12 demonstrated a similar increased risk for neonatal death (OR: 1.58) associated with SGA when using fetal growth standards. The relatively overestimated risk of neonatal mortality attributable to SGA when using neonatal growth standards as shown in the current study is likely attributable to the differences in birth weight cutoffs between the 2 growth standards. The 10th percentile cutoff differences between fetal and neonatal growth standards range between 32 g and 273 g before 34 weeks gestation.2 As a result, neonates classified as SGA using fetal growth standards at <34 weeks will be 32 g to 273 g heavier at birth than when neonatal growth standards are used, resulting in a lower risk of neonatal mortality as we observed. In addition, we have previously shown in a larger population-based study that the risk of perinatal death attributed to being born preterm SGA increased significantly only with a birth weight of less than the 3rd percentile, whereas there was no difference from AGA neonates when the birth weight was between the 3rd and the 10th percentiles.2 Respiratory morbidity attributed to RDS and neurologic morbidity attributed to IVH are the most significant complications affecting long-term outcome in premature neonates. It is generally believed that RDS is less common in SGA infants because of "accelerated pulmonary maturation",26 and some studies have supported this view.7–9 Interestingly, Piper et al10 showed a significantly higher rate of RDS in SGA infants (OR: 1.7) compared with AGA infants, but comparison by birth weight categories showed a significantly lower rate of RDS in SGA pregnancies (OR: 0.75). It has been suggested that there is a protective effect of SGA on RDS when the gestational age is controlled. Using Arbuckle’s neonatal growth standards,15 Tyson et al5 did not find the higher risk of RDS among SGA infants, but they found the risk of respiratory failure to be higher in this group. However, with the use of fetal growth standards, Ley et al12 have shown a higher incidence of RDS among preterm SGA infants born before 29 weeks gestation. Our study is the first that compared both neonatal and fetal growth standards on the same data set of preterm infants. The use of fetal growth standards not only identified a 2-fold greater number of preterm neonates classified as SGA (Table 1), but also clearly identified preterm SGA neonates as being at greater risk of neonatal respiratory morbidity when compared with neonatal growth standards. It remains to be determined if this higher respiratory morbidity in SGA neonates is attributable to a relative reduction in surfactant production, abnormal lung development, or both.
In the Vermont Oxford Network study, there was a trend toward an increased risk of IVH in preterm SGA neonates (OR: 1.13; 95% CI, 0.99–1.29).6 Bardin et al27 did not find an increased risk of IVH in SGA infants born before 27 weeks gestation. Both studies used neonatal growth standards, and their results are consistent with our findings when using neonatal growth standards to classify neonates as SGA. The use of fetal growth standards by Ley et al12 also did not show a significant difference in the incidence of IVH grade 3 and PVL between SGA and AGA infants. We combined all grades of IVH because even small IVH can be associated with adverse long-term neurologic outcome, and found that fetal growth standards identified a 2.4-fold greater number of SGA neonates with IVH when compared with neonatal growth standards (Table 1). Therefore, fetal growth standards not only identified twice as many SGA neonates than neonatal growth standards but also more than twice the number of preterm SGA neonates at risk of IVH. In contrast, the number and incidence of IVH in the AGA group using either growth curves remained unaffected. It is clear from these observations that the use of fetal growth standards were superior to neonatal growth standard to identify SGA neonates at risk of IVH. The lack of association between the risk of PVL and SGA is probably reflected in the fact that severe brain injury in the very preterm infant is multifactorial in addition to its relatively rare occurrence.11
It was of interest that the increased risk of ROP associated with SGA was well-maintained when using neonatal or fetal growth standards, providing further evidence of enhanced detection rate of SGA neonates at risk of adverse outcome with fetal growth curve applied to premature neonates. SGA infants are known to be at higher risk for NEC.28 We have demonstrated an increased risk of NEC in SGA infants with the use of neonatal growth standards, and a trend toward increased risk of NEC when fetal growth standards were used.
We acknowledge that our study has some limitations attributable to the retrospective analysis of data. It has also been suggested that ultrasonographically derived measurement of fetal weight provides an estimate of weight and not a precise absolute measurement.29 Fetal growth standards are used for both sexes, whereas neonatal growth standards are gender-specific. However, gender was included and corrected for in the multiple logistic regression analysis. Serial in utero estimates of fetal weight were not available in our database. Neonatal birth weight curves including preterm neonates are derived from abnormal pregnancies and may not represent intrauterine growth trajectory of fetuses born at term.2,30,31 However, the strength of the study is that we have tested our hypothesis based on the analysis of a comprehensive perinatal database collected prospectively and consistently throughout the study period. It is also the first study of a large cohort of preterm infants born in a single tertiary care center comparing the effect of reclassification of neonates as being SGA using the current gold standard of neonatal growth curves compared with fetal growth standards in relation to neonatal outcome.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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This study has demonstrated that fetal growth standards are more appropriate than currently used neonatal growth standards for the identification of preterm SGA neonates at risk of adverse neonatal outcome, particularly respiratory morbidity and IVH, even after correction for antenatal administration of glucocorticoids. Future studies are needed to improve antenatal detection of growth-restricted fetuses at higher risk for adverse neonatal outcomes.
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ACKNOWLEDGMENTS |
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We are thankful to Larry Stitt for his statistical assistance.
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FOOTNOTES |
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Received for publication Nov 20, 2002; Accepted Jan 14, 2003.
Reprint requests to (O.d.S.) St Joseph’s Health Care London, 268 Grosvenor St, London, Ontario, N6A 4V2, Canada. E-mail: odasilva{at}uwo.ca
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