Original Article

Short-term Morbidities of Moderate and Late Preterm Infants Neonatale Morbiditäten bei Frühgeborenen 32–36 Schwangerschaftswochen


A. Scheuchenegger1, E. Lechner2, G. Wiesinger-Eidenberger2, M. Weissensteiner2, O. Wagner2, W. Schimetta3, B. Resch1



Research Unit for Neonatal Infectious Diseases and Epidemiology, Division of Neonatology, Department of Paediatric and Adolescent Medicine, Medical University of Graz, Austria 2 Children’s and Maternity Hospital Linz, Neonatology, Linz, Austria 3 Applied Systems Research, Johannes Kepler University, Linz, Austria

Key words ▶ moderate preterm ● ▶ late preterm ● ▶ short-term morbidities ● ▶ neonatal intensive care unit ●



Objective: To determine (1) the association between neonatal morbidity and gestational age and (2) the impact of pre-existing maternal medical conditions, pregnancy and birth complications on neonatal outcome in moderate and late preterm infants (32–36 completed weeks). Methods: Retrospective single-centre cohort study including all moderate and late preterm infants without congenital anomalies born at the Children’s and Maternity Hospital Linz, Austria, between January 2007 and June 2010. Stepwise regression analysis was used to determine significant associations between morbidities, maternal and perinatal complications and the gestational age. Results: Of 870 infants included the incidence of neonatal morbidities increased from 24 % at 36 weeks to 43 % at 35 weeks’, 55 % at 34 weeks’, 75 % at 33 weeks’ and 93 % at 32 weeks’ gestation. Infants at 32 weeks had a 4-fold (RR: 3.88; 95 % CI: 1.87–8.06) increased risk compared with those at 36 weeks, and infants of 32 weeks were 16 times (RR: 16.01; 95 % CI: 9.82–26.09) more likely to be admitted to the NICU than infants of 36 weeks’. Hyperbilirubinaemia (29 %) and respiratory morbidity (14.3 %) were the most common neonatal diagnoses. Intrauterine growth restriction, preeclampsia, preterm premature rupture of the membranes, lack of antenatal steroid administration, antepartum haemorrhage, multiple pregnancy and male gender were all associated with any kind of neonatal morbidity, admission rate to the NICU and length of hospital stay (p < 0.05). Conclusion: Nearly half of all infants suffered from any morbidity, and several risk factors were identified being significantly associated with NICU admission rate and length of hospitalization.

Hintergrund: Ziel dieser Arbeit ist es, die Morbidität von moderaten und späten Frühgeborenen (320/7–366/7 Gestationswochen [GW]) während des Krankenhauserstaufenthalts, die mit der jeweiligen Gestationswoche einhergeht, sowie den Einfluss von mütterlichen und perinatalen Komplikationen darauf, zu untersuchen. Methode: Retrospektive Single-centre-Kohortenstudie mit Frühgeborenen von 32/0 bis 36/6 GW ohne kongenitale Anomalien, geboren an der Landes-Frauen- und Kinderklinik Linz zwischen 2007 und Juni 2010. Logistische Regressionsanalyse wurde angewendet, um den Zusammenhang zwischen Morbidität, mütterlichen und perinatalen Komplikationen und dem Gestationsalter festzustellen. Ergebnisse: 870 Frühgeborene wurden eingeschlossen. Die Inzidenz der neonatalen Morbidität stieg mit abnehmendem Gestationsalter von 24 % nach 36, auf 43 % nach 35, auf 55 % nach 34, auf 75 % nach 33 und auf 93 % nach 32 GW. Am häufigsten trat eine therapiebedürftige Hyperbilirubinämie (29 %) auf, gefolgt von respiratorischen Problemen (14 %). Unter 10 % der Kinder hatten Hypoglykämien. Ein niedrigeres Gestationsalter war ein unabhängiger Risikofaktor für eine erhöhte Morbidität und einen längeren Aufenthalt im Krankenhaus bzw. auf der Intensivstation. Perinatale und mütterliche medizinische Komplikationen (Lungenreifungsinduktion, komplizierte Schwangerschaft, PPROM, Dystrophie, Mehrlingsgeburt, männliches Geschlecht) nahmen Einfluss auf das Risiko für einige Morbiditätsgruppen. Schlussfolgerung: Frühgeborene zwischen 32 und 37 Gestationswochen haben ein hohes Risiko für neonatale Erkrankungen, wobei ein niedrigeres Gestationsalter bei Geburt das Morbiditätsrisiko unabhängig von anderen Faktoren erhöht.

Bibliography DOI http://dx.doi.org/ 10.1055/s-0033-1355394 Published online: 2013 Klin Padiatr © Georg Thieme Verlag KG Stuttgart · New York ISSN 0300-8630 Correspondence Prof. Dr. Bernhard Resch Paediatrics Medical University of Graz Auenbruggerplatz 30 8036 Graz Austria Tel.: + 43/316/385 81134 Fax: + 43/316/385 2678 [email protected]

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Schlüsselwörter ▶ späte Frühgeborene ● ▶ mäßig Frühgeborene ● ▶ neonatale Morbiditäten ● ▶ neonatale Intensivstation ●

Original Article

Preterm birth is the most frequent risk factor for morbidity and mortality during the first year of life [27] and affects approximately one of 14 (7.2 %) births in Europe [7] and one of 8 (12.5 %) in the USA [16] each year. The majority of preterm-related mortality and morbidity occurs among very premature infants ( < 32 gestational weeks’ gestation); therefore research focussed on this patient group for a long time [27]. However, increased attention has recently been given to the moderate (32/0–33/6 weeks’ gestation) and late (34/0–36/6 weeks’ gestation) preterm infants regarding health and economic outcomes [28]. Although their risk for neonatal morbidity is much lower, this group of premature infants accounts for approximately 85 % of all preterm births in both Europe [7] and the USA [28]. Moderate and late preterm infants are, like preterm infants in general, physiologically, anatomically and metabolically immature [28]. Compared with term infants, they are more prone to respiratory distress, hypothermia, hypoglycaemia, hyperbilirubinaemia, apnoea, seizures, and feeding problems, as well as longer hospital stays and higher rates of rehospitalisation [24, 30]. So far no studies have examined neonatal morbidity, rates of NICU admission and length of hospital stays of moderate and late preterm infants in the German-speaking area. However, by comparison of different study groups and countries, regional variations may emerge [5]. Therefore, we conducted a retrospective study to define the short-term outcomes associated with each gestational week (32–36 completed weeks), and to examine associations between pre-existing maternal medical conditions, pregnancy and birth complications among moderate and late preterm infants.

Patients and methods

This is a retrospective cohort study of moderate and late preterm infants (32/0–36/6 weeks’ gestation) who were born at the Children’s and Maternity Hospital Linz in Austria, a tertiary teaching hospital covering 3 300 births per year. Infants born between January 2007 and June 2010 were identified using the obstetric electronic medical record database of the Children’s and Maternity Hospital Linz. This secure database contains pertinent information on all mothers and neonates delivered at the Children’s and Maternity Hospital Linz. Using the medical record number and gestational age of each neonate based on best obstetric estimate, we reviewed 10 824 records (480 records of infants of 23–31 6/7 weeks’, 9 399 records of infants 37–40 weeks’, and 945 records of infants of 32–36 6/7 weeks’ gestational age). Inclusion criterion was a gestational age between 32 0/7 and 36 6/7 completed weeks’ gestation. Exclusion criteria were 1) incomplete medical records of mother or child, 2) major congenital anomalies, and 3) genetic aberrations. For the exploratory data analysis we used logistic and multiple regression analyses. The main outcome measures were used as dependent variables while the covariates (maternal conditions) were used as independent variables. For relative risks (RR) 2-sided 95 % confidence intervals (95 % CI) were calculated. Statistical analyses were performed using the R 2.14.1 statistical package und SPSS18 statistical software (SPSS Inc., Chicago, USA). No adjustment for the type I error was made. Therefore the Scheuchenegger A et al. Short-term Morbidities of Moderate … Klin Padiatr

concerning p-values are only descriptive. The study was approved by the local ethics committee.

Maternal data

Data were collected regarding maternal age and complications of pregnancy including hypertensive diseases of pregnancy (HDP), diabetes, chorioamnionitis, placental abruption, placenta praevia, preterm and premature rupture of membranes (PPROM), oligohydramnion, corticosteroids for induction of lung maturation and presence of intrauterine growth restriction (IUGR). Chronic arterial hypertension, pregnancy-induced hypertension, pre-eclampsia and eclampsia were all added up to HDP, and gestational and pre-existing diabetes mellitus to diabetes. PPROM referred to rupture of membranes before 37 weeks of gestation. Chorioamnionitis was defined as infection or suspected infection of the amniotic cavity as determined by clinical criteria by the attending physician. Lung maturation was induced in mothers with imminent preterm birth after 24 through 33 6/7 weeks’ gestation. Small-for-gestational-age newborns were identified when birth weight was below the 10th percentile according to neonatal growth standards.

Perinatal and neonatal data

Births were classified as moderate and late preterm on the basis of the calculated estimate of gestational age in completed weeks as reported on the birth certificate. The gestational age was assessed on the basis of the mother’s last menstrual period, as confirmed or modified when necessary by routine early antenatal ultrasound examination. Pertinent neonatal information included mode of delivery, gestational age, sex, Apgar scores, umbilical artery pH and birth weight. Neonatal outcome measures included respiratory morbidity, hyperbilirubinaemia with need for phototherapy, hypoglycaemia, sepsis, need for parenteral nutrition, necrotizing enterocolitis (NEC), central nervous system disorders, admission to the neonatal intensive care unit (NICU), and duration of hospitalization. Respiratory morbidity was defined as any of the following: the presence of either respiratory distress syndrome (RDS), transient tachypnea of the newborn (TTN) or need for oxygen and/or ventilatory support. RDS was diagnosed in babies with respiratory distress (requirement for oxygen supplementation due to tachypnea, grunting, nasal flaring, retractions and/or cyanosis) together with chest X-ray and blood gas analysis. TTN was diagnosed in babies with clinical signs of respiratory distress in the first hours of life and radiographic findings of perihilar streaking, fissure oedema, and congestion. Hyperbilirubinaemia was defined as need for phototherapy based on laboratory measurement of serum bilirubin concentration [14]. Hypoglycaemia was defined as blood glucose level < 40 mg/dl. Sepsis was defined as blood culture and/or clinical and laboratory (C-reactive protein > 10 mg/L) positive bacterial infection. Clinical signs of sepsis were defined as the presence of 3 or more of the following apnoea/tachypnoea ( > 60/min), nasal flaring, retractions, cyanosis, respiratory distress; bradycardia ( < 100/min)/tachycardia ( > 180/min); hypotonia, seizures; poor skin colour; capillary refilling time > 2 s; irritability/lethargy [26]. NEC was classified according to Bell’s criteria [3]. Central nervous system (CNS)

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Original Article


Of 945 preterm infants initially enrolled, 74 (7.8 %) were excluded due to congenital anomalies and morbidities not caused by immaturity (e. g. detoxification symptoms after maternal addiction during pregnancy or rhesus isoimmunisation) and one for incomplete medical record. Therefore, 870 moderate and late preterm neonates were finally included in the ▶ Table 1. Modstudy. Demographic characteristics are listed in ● erate and late preterm infants born at our hospital constituted approximately 9 % of all deliveries and 61 % of preterm deliveries between January 2007 and June 2010. Overall, 406 (46.7 %) infants suffered from any neonatal morbid▶ Fig. 1). The rate was lowest with 24 % among the infants of ity (● 36 weeks’ gestational age and highest with 93 % among 32 weeks’ gestational age. Infants at 32 weeks’ gestational age had a 4-fold (RR: 3.88; 95 % CI: 1.87–8.06) increased risk for any neonatal morbidity compared with those at 36 weeks’ gestational age; those born at 33, 34, and 35 weeks’ gestational age, respectively, a 3-fold (RR: 3.13; 95 % CI: 1.54–6.35), 2–fold (RR: 2.31; 95 % CI: 1.13–4.70), and 1.8-fold (RR: 1.81; 95 % CI: 0.89–3.70) increased risk for any neonatal morbidity, respectively. Details of neonatal ▶ Table 2. 14% of the infants morbidities are depictured in ● exhibited nasal CPAP ventilation. Need for mechanical ventilation and surfactant replacement therapy were low (2.5 and 1.5 %, respectively) as were severe complications of neonatal intensive care ( < 0.5 %). No death occurred during primary hospitalisation. There was a direct relationship between younger gestational age and higher rates of neonatal morbidities, and nearly a quarter of all infants had to be hospitalized at the NICU. Hypoglycaemia was observed more frequently in infants of 33 and 34 weeks’ gestational age. Hyperbilirubinaemia (29 %), respiratory morbidity (14.3 %), and need for total parenteral nutrition (13.7 %) were the most common neonatal diagnoses. The median length of hospital stay of the whole population was 5 days; approximately 23 % (201 infants) of all included infants were hospitalized at the Neonatal Intensive Care Unit (NICU). The median length of stay declined linearly from 32 to 36 weeks’ gestational age with 26 days for infants of 32 weeks’, 14 days for infants of 33, 9 days for infants of 34, 5 days for infants of 35, and 4 days for infants of 36 weeks’ gestational age. Infants of 32 weeks’ gestation were 16 times (RR: 16.01; 95 % CI: 9.82–26.09) more likely to be admitted to the NICU than infants of 36 weeks’ gestation. There was only one infant suffering from NEC that was born at 32 weeks’ gestational age. Severe adverse conditions – defined as IVH, cPVL, NEC, BPD or ROP- were rare ( < 0.5 %); there occurred no death before discharge home. Lung maturation with prenatal corticosteroids was performed in 319 cases (36.7 %) with 79 % among births of 32 weeks’, 85.3 % among births of 33 weeks’, 52.3 % among births of 34 weeks’, 22.3 % among births of 35 weeks’ and 11.8 % among births of 36 weeks’ gestation. A rate of 19.7 % presented with respiratory problems (RDS, TTN, and need for oxygen). The mean maternal age was 30.0 ± 5.5 (SD) years. Obstetric factors commonly associated with preterm delivery included PPROM in 43.9 %, scheduled caesarean section in 12 %, pre-eclampsia in 6 %, antenatal haemorrhage in 3 %, and pathological cardiotocography in 3 % of cases.

Table 1 Demographic data, maternal medical conditions, and pregnancyrelated characteristics of our study cohort (n = 870). sex male 462 female 408 gestational age (weeks) 81 (9) 320/7–326/7 95 (11) 330/7–336/7 174 (20) 340/7–346/7 206 (24) 350/7–356/7 314 (36) 360/7–366/7 birth weight (g) 2 360 ± 504 premature rupture of membranes 382 (44) Caesarean section 518 (60) multiple gestation 304 (35) antenatal steroids 319 (37) maternal age 30.0 (26.4–34.2) maternal medical conditions and pregnancy complications HDP (chronic hypertension, pregnancy-induced 117 (13) hypertension, eclampsia) diabetes 66 (8) antepartum haemorrhage (placenta praevia, 37 (4.3) placenta abruption) oligohydramnion 30 (3.4) Data are mean ± standard deviation, n ( %), or median (interquartile range) HDP: hypertensive diseases of pregnancy

100 % 93 % 90 % 80 % 70 % 60 % 50 % 40 % 30 % 20 % 10 % 0% 32

75 % 55 % 43 % 24 %

33 34 35 gestational age in weeks


Fig. 1 Percentage of neonatal morbidities of 870 moderate and late preterm infants.

The regression analyses showed clear correlations between every single observed morbidity and gestational age (p < 0.05). The lower the gestational age at birth the higher was the proportion of infants who suffered from any neonatal morbidity regardless of maternal medical condition. 209 mothers (24 %) had reported maternal medical conditions (hypertensive disorders of pregnancy, diabetes, renal/gastrointestinal diseases, and malignant tumours). Infants who were exposed to antenatal hemorrhage or oligohydramnion more frequently required parenteral nutrition (p < 0.05), had longer stays in the NICU (p < 0.001) and less frequently required phototherapy due to hyperbilirubinaemia. There was a clear correlation between longer stays in the NICU and HDP (p < 0.05). After the administration of antenatal steroids infants were substantially shorter in the NICU and needed more frequently only noninvasive respiratory support (p < 0.05). Intrauterine growth restriction infants more frequently had hypoglycaemia (p < 0.05), needed parenteral nutrition (p < 0.001) and were longer Scheuchenegger A et al. Short-term Morbidities of Moderate … Klin Padiatr

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morbidity included seizures, intraventricular haemorrhage (any grade), white matter disease, and any other neurologic abnormalities.

Original Article

Table 2 Pertinent neonatal outcomes as a function of gestational age at delivery. Outcome hyperbilirubinaemia requiring phototherapy respiratory morbidity IRDS mechanical ventilation nasal CPAP surfactant parenteral nutrition length of parenteral nutrition (days) hypoglycaemia neonatal sepsis NICU admission length of NICU stay (days) length of hospital stay (days) ROP

32 weeks

33 weeks

34 weeks

35 weeks

36 weeks

n = 81

n = 95

n = 174

n = 206

n = 314

43 (53.1) 43 (53.1) 15 (18.5) 4 (4.9) 38 (46.9) 4 (4.9) 52 (64.2) 4 (0–6) 10 (12.3) 40 (49.4) 66 (81.5) 4 (2–8) 26 (20–32) 2 (2.5)

42 (44) 22 (23.2) 6 (6.3) 5 (5.3) 24 (25.3) 2 (2.1) 29 (30.5) 0 (0–2) 19 (20) 19 (20) 40 (42.1) 0 (0–3) 14 (9–21) 1 (1.1)

48 (28) 39 (22.4) 12 (6.9) 9 (5.2) 33 (19) 6 (3.4) 25 (14.4) 0 (0–0) 28 (16.1) 15 (8.6) 57 (32.8) 0 (0–2,75) 9 (5–18) 5 (2.9)

64 (31) 7 (3.3) 4 (1.9) 3 (1.5) 15 (7.3) 1 (0.5) 9 (4.4) 0 (0–0) 13 (6.3) 10 (4.9) 22 (10.7) 0 (0–0) 5 (4–7) 0*

55 (18) 2 (0.6) 0 1 (0.3) 8 (2.5) 0 4 (1.3) 0 (0–0) 10 (3.2) 3 (1) 16 (5.1) 0 (0–0) 4 (3–5) 0*

IRDS: infant respiratory distress syndrome, CPAP: continuous positive airway pressure, NICU: neonatal intensive care unit, ROP: retinopathy of prematurity *not observed in this age cohort

hospitalized (p < 0.001). Longer hospitalizations were also assessed in multiple gestation (p < 0.05). However, multiples less frequently required phototherapy due to hyperbilirubineamia and were less frequently affected by severe morbidities like brain haemorrhage or sepsis. Phototherapy was more frequently required for male infants (p < 0.05). 33 % of the male infants and 25 % of the female infants required phototherapy. Infants who were exposed to PPROM were more likely to require phototherapy (p < 0.001), but were less likely to necessitate parenteral nutrition. Of interest, diabetes seemed to have no effect on the morbidity for our study cohort. Maternal age was uniformly distributed and as well had no influence on neonatal morbidity.


The major findings of our study were first that the risk for any short-term morbidity in moderate and late preterm infants is clearly related to gestational age, and the most commonly observed morbidities among our study subjects were hyperbilirubinaemia, respiratory morbidity and need for parenteral nutrition. Published data relating to preterm infants’ morbidity based on single gestational weeks is limited. Numerous previous studies compared late-preterm infants’ neonatal outcome with term infants [11, 19, 32, 33]. However, the differences between those born at 32–36 weeks suggest that it is inappropriate to regard moderate and late-preterm infants as a homogeneous group with respect to neonatal morbidity and mortality [35]. The incidence of any respiratory condition steadily decreased from the 32 weeks’ gestation group (48.1 %) to the 36 weeks’ gestation group (2.9 %), the incidence of RDS from 18.5 to 1.9 % at 35 weeks’ gestation with substantial differences between the age groups. The overall incidence of respiratory morbidity and RDS with 14.3 % and 4.3 %, respectively, compare well to other studies [1, 17, 19]. In an US study including 19 334 infants born at 34–36 completed weeks during 2002–2008, Hibbard et al. [4] found higher incidences of RDS and mechanically ventilated infants as compared with our study. Some differences reflect regional variations [31], others different approaches regarding the use of Scheuchenegger A et al. Short-term Morbidities of Moderate … Klin Padiatr

nasal CPAP or mechanical ventilation as primary ventilation strategies [1, 4, 6, 20]. The rate of surfactant administration was low (1.5 %), and with increasing gestational age ( > 32 weeks) other aetiologies for neonatal respiratory failure predominated (e. g. pneumonia, sepsis, asphyxia, pulmonary haemorrhage, and meconium aspiration syndrome) [12]. The overall rate of hypoglycaemia in our study was 9 %, which is similar to rates reported by Melamed et al [19]. However, some previously reported rates were markedly higher (16–35 %) [1, 2, 18]. Our finding of higher rates of hypoglycaemia in infants of 33 and 34 weeks’ gestation, but not of 32 weeks’ gestation might be related to the fact that more infants of 32 weeks’ gestational age primarily received intravenous glucose infusions or parenteral nutrition and therefore experienced less hypoglycaemia. Hyperbilirubinaemia requiring phototherapy was the most common morbidity in our study population (29 %); similar to the findings of Medoff-Cooper et al [18]. Preterm neonates have developmentally immature liver enzymes and a slower maturation of hepatic bilirubin uptake and bilirubin conjugation compared with full-term infants [10]. Melamed et al [19]. reported a rate of 18 % in their study cohort of late preterm infants of 34/0– 36/6 weeks’ gestation. Their finding of lower rates of hyperbilirubinaemia with each increasing gestational week is well comparable. Several divergent results have been published by other authors [1, 2, 17] that partly might be explained by different criteria for initiation of phototherapy [15, 21]. Male sex was a predictor for hyperbilirubinaemia requiring phototherapy; a finding, which was also reported in previous studies [22, 34]. Review of the literature [8] suggests a clear association between PPROM and perinatal infection. Infection is an established risk factor for haemolysis which may have resulted in higher rates of hyperbilirubinaemia. However, we do not have an explanation for the lower rates of parenteral nutrition after PPROM. Shapiro-Mendoza et al. [29] found that both lower gestational age and, to a lesser extent, maternal medical conditions were each independent risk factors for adverse neonatal outcome. We could show an influence of prenatal haemorrhage, oligohydramnion and hypertensive disorders in pregnancy on the neonatal morbidity.

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Data are n ( %), or median (interquartile range)

Intrauterine growth restriction has been related to higher rates of morbidity and mortality during the neonatal period [23], which matches our findings of higher rates of hypoglycaemia, hyperbilirubinaemia and longer hospital stays. Although outcomes for moderate and late preterm twins are generally regarded as favourable, their neonatal morbidity is higher compared with singleton pregnancies [25]. In our study multiple pregnancies resulted in longer stays at the hospital. However, we do not have a plausible explanation for our observation of less frequent requirement of phototherapy due to hyperbilirubinaemia and lower incidences of IVH and sepsis for multiples. Our study has several limitations. The most important limitation is the retrospective design of the study, and furthermore, the relatively small sample size. Our results result from a single centre analysis and may therefore not be generally representative. Due to variations of structural characteristics even in tertiary care perinatal units in Europe [9] patterns of care, frequency of initiating interventions or noting conditions suggesting morbidity and the criteria for discharge may differ between hospitals and countries. However, the lengths of stay and frequencies of NICU admission are similar to those reported by others [13, 31]. In conclusion, our findings indicate that the risk for neonatal morbidity among moderate and late preterm infants substantially increases with each earlier week of gestation. The gestational age was identified as the strongest factor associated with adverse short-term outcome, and the rate of NICU admissions was remarkable high even in the late preterm infants group.

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Scheuchenegger A et al. Short-term Morbidities of Moderate … Klin Padiatr

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Original Article

Short-term morbidities in moderate and late preterm infants.

To determine (1) the association between neonatal morbidity and gestational age and (2) the impact of pre-existing maternal medical conditions, pregna...
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