The abdominal circumference was the principal fetal measurement upon which the diagnosis of IUGR was made. The diagnosis in utero received additional confirmation by the fact that all infants in the study also had abnormal umbilical artery velocimetry findings.
Figure 3 presents the abdominal circumference data measured by ultrasonography within 7 days from delivery. All IUGR infants were below the 10th percentile. The mean±SD percent reduction of the abdominal circumference compared with the 10th percentile of the reference values11 was significantly higher in the IUGRSGA (21.1±5.8%) when compared with the IUGRAGA (11.3±2.8%; P<.001).
Table 2 presents maternal age, height, prepregnancy weight, BMI, and weight increase in pregnancy of AGA and IUGR mothers. No differences were present in any of these variables. It is worth noting that all IUGRAGA mothers were primigravid (P<.001 both compared with AGA and IUGRSGA).
The number of women who started their pregnancy as low risk (absence of familial, personal, or obstetric pathologies) was 47 of 79 in the AGA group, 14 of 25 in the IUGRAGA group, and 16 of 28 in the IUGRSGA group (P=.8). During pregnancy, 50 of 79 control AGA mothers had no pathology other than premature labor or preterm premature rupture of the membranes compared with 10 of 53 IUGR mothers (five IUGRAGA and five IUGRSGA; P<.001).
On the contrary, the incidence of hypertensive disorders was significantly higher in IUGR (35 of 53) than in AGA (13 of 79; P<.001) mothers, a difference that persisted when the individual IUGR groups were considered (19 of 25 IUGRAGA; 16 of 28 IUGRSGA). Among multiparas, a previous stillbirth or IUGR was present in 6 of 19 IUGR compared with 3 of 28 AGA pregnancies (P=.1).
Table 3 presents the gestational age, birth weight, placental weight, fetal/placental weight ratio, neonatal length, head circumference, ponderal index, body mass index, and brain body weight ratio in AGA and IUGR for the IUGR group as a whole and subdivided into the birth weight–related groups. Gestational age was significantly higher in controls (P<.003): when corrected for gestational age, brain–body weight ratio, and fetal/placental ratio, were significantly lower in AGA compared with IUGR, whereas all other measures were significantly higher in AGA compared with IUGR. Similarly, all body size measurements were also greater for AGA compared with the IUGR groups separately. These measurements included birth weight, placental weight, neonatal length, head circumference, neonatal pulsatility index, and BMI, which were significantly higher in AGA than in IUGRAGA and IUGRSGA, whereas, again, brain–body weight ratio and fetal/placental weight ratio were significantly lower in AGA.
Among IUGR, birth weight, placental weight, neonatal length, and neonatal BMI were significantly higher in IUGRAGA than in IUGRSGA, whereas brain–body weight ratio was significantly increased in IUGRSGA, although we found no differences in placental weight, fetal/placental weight ratio, head circumference, and neonatal ponderal index.
Forty-seven of 79 AGA mothers had cesarean deliveries compared with 53 of 53 IUGR (P<.001). In most IUGR pregnancies (85%), cesarean delivery was performed for fetal indication.
Twenty-nine of 79 AGA newborns had a 5-minute Apgar score of 7 or less when compared with 35 of 53 IUGR (P<.001); no differences were present between IUGR groups (16 of 25 IUGRAGA and 19 of 28 IUGRSGA; P=.8). The number of newborns requiring assisted ventilation was significantly higher in the IUGR group when compared with the AGA (75.5% compared with 40.5%; P<.001), with no differences between IUGRs (Fig. 4). The number of fetuses receiving antenatal corticosteroids was significantly higher in IUGR (51 of 53 compared with 23 of 79; P<.001) as was the number of neonates receiving surfactant after delivery (49 of 53 compared with 50 of 79; P<.001).
Forty-nine of 79 AGA and 49 of 53 IUGR were admitted to the NICU (P<.001). One of 79 AGA and 6 of 53 IUGR newborns (one IUGRAGA and five IUGRSGA) died within 28 days after delivery (P<.02). Neonatal major and minor morbidity is presented in Figure 4. More than one third of the control AGA and 23 of 53 IUGR newborns had major complications, whereas 68.4% of AGA had minor complications when compared with 85% IUGR newborns; none of these differences was significant when corrected for gestational age. Similarly, no differences were present in the individual IUGR groups. Only 6 of 53 IUGR had no postnatal complications when compared with 23 of 79 AGA. Pulmonary dysplasia, retinopathy of prematurity stage 3 or more, and neurologic sequelae at the time of discharge were present in 5 of 79 AGA and 7 of 53 IUGR (ns).
This article presents the obstetric and neonatal outcome in IUGR pregnancies diagnosed using intrauterine fetal growth curves and velocimetry without regard to the neonatal growth curves. The study clearly demonstrates that neonatal morbidity and mortality are similar in IUGR of the same clinical severity, whether or not they could be defined appropriate or small for gestational age according to the neonatal growth standards.
The issue of whether fetal or neonatal growth curves should be used when assessing weight at birth has been addressed by other authors.16,17 Zaw et al18 showed that fetal growth standards are better in identifying infants at increased risk of respiratory morbidity and intraventricular hemorrhage among preterm SGA infants compared with neonatal standards. Similarly, Clausson et al19 showed that the use of customized birth weight standards increases identification of fetuses at risk of stillbirth, neonatal death, and Apgar score less than 4 at 5 minutes when compared with population-based birth weight standards.
However, we have reviewed the literature using PubMed restricted to English language from 1970 to May 2008, using the key words intrauterine growth charts, neonatal growth charts, abnormal doppler, fetal growth restriction, and fetal biometry and were unable to find any other studies that had the dual characteristics of 1) a prospective study of IUGR and 2) met the stringent requirements of diagnosis of IUGR made in utero based upon both fetal growth and the presence of abnormal velocimetry and related these cases to neonatal outcome. Furthermore, to avoid growth restriction based solely upon biometry, which could have included “normal small” neonates, we have included in our study only fetuses with abnormal pulsatility index of the umbilical artery, ie, the more severe, as we have shown previously (Marconi AM, Ronzoni S, Vailati S, Bozzetti P, Pardi G, Battaglia FC. Neonatal morbidity and mortality in intrauterine growth restricted (IUGR) pregnancies according to clinical severity [meeting abstract]. Pediatr Res 2004;55:476A).5,20 These dual criteria should have avoided the interference of potential confounding factors such as maternal height, weight, ethnicity, parity, and newborn’s gender.4 In our study, as in Zaw’s,18 there was a large birth weight difference between fetal and neonatal growth standards. This finding is strengthened by the fact that we have used standards developed for our population both for intrauterine growth11 and for neonatal growth.15
It is well recognized that the assessment of fetal growth is a fundamental component of good antenatal as well as postnatal care due to its consequences for perinatal outcome1 and adult health.21 It is now acknowledged that there are ethnic differences that should be taken into account when analyzing perinatal outcomes.4 Also, the issue of whether customized compared with population-based growth curves should be used16 has been debated. The customized growth standards are useful in taking into account all known constitutional factors affecting growth in individual fetuses. But both of these effects are minor when one uses both fetal biometry and fetal velocimetry data.
This study highlighted several facts. First, there were no relevant prepregnancy differences for mothers in the control AGA group compared with those in the IUGR groups; more than one half in each group started pregnancy considered at low risk. On the other hand, most IUGR mothers developed hypertension in pregnancy, with no differences between IUGRAGA and IUGRSGA mothers.
The second observation is that we did not find significant differences in neonatal outcome between AGA and IUGR infants, most likely due to two factors: 1) that IUGR fetuses were followed prospectively and delivered to minimize morbidity and mortality22 and 2) that AGA infants were gestational age–matched and thus were preterm infants with significant morbidity and mortality. The differences in morbidity and mortality are mainly due to IUGRSGA. All IUGR fetuses of group 2 and 3 exhibited abnormal umbilical pulsatility index measurements of the umbilical artery. In addition, as shown in Table 3, they had birth weights, placental weights, neonatal lengths, head circumferences, ponderal indexes, and body mass indexes that were significantly lower and fetal/placental weight ratios and brain–body weight ratios that were significantly higher than AGA fetuses whose intrauterine growth was normal. Also, they required NICU admission more frequently than fetuses with normal intrauterine growth.
The issue of whether perinatal outcome is different in preterm AGA when compared with SGA has been debated for many years. However, as reported above, only recently the question of the growth standards to be used in comparing different populations and the criteria for diagnosis of intrauterine growth restriction prenatally has begun to be addressed. The results of the present prospective study are in agreement with the results of larger retrospective studies3,18 in showing not only that IUGR increases perinatal morbidity and mortality, but also that perinatal outcome is correlated with the degree of clinical severity (Marconi AM, Ronzoni S, Vailati S, Bozzetti P, Pardi G, Battaglia FC. Neonatal morbidity and mortality in intrauterine growth restricted (IUGR) pregnancies according to clinical severity [meeting abstract]. Pediatr Res 2004;55:476A). They also reinforce the conclusion that neonatal birth weight/gestational age percentile curves are misleading in detecting low birth weight infants and should be used only when obstetric data are unavailable. The results of the present study also point out the need of a truly perinatal approach (ie, joint obstetric and neonatal approach) in the clinical management of these patients if optimal medical care is to be provided.
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© 2008 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved.
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