PEDIATRICS Vol. 120 No. 4 October 2007, pp. e788-e794 (doi:10.1542/peds.2006-3765)
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ARTICLE |
Postdischarge Infant Mortality Among Very Low Birth Weight Infants: A Population-Based Study
a Department of Neonatology, Bnai Zion Medical Center, Bruce Rappaport Faculty of Medicine, Technion–Israel Institute of Technology, Haifa, Israel
b Women and Children's Health Research Unit, Gertner Institute, Tel Hashomer, Israel
c Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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OBJECTIVE. The objective of this study was to identify factors that were associated with death after discharge from the NICU of very low birth weight infants in a population-based study.
METHODS. From a national cohort of 13430 very low birth weight infants who were born in Israel from 1995 to 2003, 10602 infants were discharged from the hospital and composed the study population. Demographic and clinical data regarding the pregnancy, delivery, and neonatal course were obtained from the Israel national very low birth weight infant database. Data on each case of death during the postdischarge period until 1 year of age were provided by the Ministry of Health from national linked birth and death certificates. Univariate analyses and a multivariable logistic regression analyses were performed to examine the perinatal and neonatal risk factors for postdischarge death.
RESULTS. The postdischarge mortality rate was 7.5 per 1000 (80 of 10602 infants discharged from the hospital). The death rate was significantly higher in non-Jewish infants, infants who were born to young mothers, and infants who were born to low-educated mothers. After adjustment for demographic characteristics and perinatal and neonatal variables, postdischarge mortality was independently associated with congenital malformations, neonatal seizures, necrotizing enterocolitis, and bronchopulmonary dysplasia.
CONCLUSION. Although the postdischarge death rate was relatively low in our cohort of very low birth weight infants, attention should be focused on the subgroups of infants who are at higher risk to decrease their mortality further.
Key Words: discharge • infant mortality • VLBW infants
Abbreviations: SIDS—sudden infant death syndrome • VLBW—very low birth weight • IMR—infant mortality rate • SGA—small for gestational age • RDS—respiratory distress syndrome • BPD—bronchopulmonary dysplasia • PDA—patent ductus arteriosus • NEC—necrotizing enterocolitis • IVH—intraventricular hemorrhage • PVL—periventricular leukomalacia • OR—odds ratio • CI—confidence interval • ICH—intracranial hemorrhage
Postneonatal mortality is defined as death that occurs between 28 and 364 days of age. Sudden infant death syndrome (SIDS) and congenital malformations are the predominant causes of postneonatal mortality.1 Callaghan et al,2 however, recently assessed the contribution of preterm birth to infant mortality in the United States, suggesting that preterm birth accounted for at least one third of deaths and was the most frequent cause of infant death. Only 7% of deaths attributable to preterm birth were postneonatal. The leading causes, accounting for 60% of postneonatal deaths that were attributable to preterm birth, were "chronic respiratory disease originating in the perinatal period" and gastrointestinal disorders, especially "acute vascular disorders of the intestine." Among white infants, very low birth weight (VLBW) was associated with an eightfold excess odds for postneonatal mortality compared with the normal birth weight group.3 Furthermore, in a study by Callaghan et al,2 95% of deaths that were attributable to preterm birth occurred in infants who were born at <32 weeks’ gestation and weighed <1500 g.
The mean length of hospitalization of VLBW infant survivors is reportedly 
60 days,4 and VLBW infants are routinely hospitalized beyond 28 days.5 A lot of medical, emotional, and financial effort is invested in these infants during their prolonged stay in the NICU. Whereas neonatal and infant mortality rates (IMRs) are well documented, there are only scarce data in the literature on the postdischarge IMR (until 1 year of age) and the determinants of postdischarge mortality among VLBW infants.
Identification of risk factors that are associated with postdischarge death in the vulnerable period of early infancy may enable the introduction of intervention programs to try to reduce its rate. A previous study found that mortality risk was statistically increased for infants who were NICU graduates, of low birth weight, preterm, or small for gestational age (SGA).6 Therefore, this may be an important target population for such programs. The aim of our study was to determine the rate and to identify potential risk factors for postdischarge death in a population-based study of VLBW infants in Israel.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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This study is based on analysis of data collected by the Israel Neonatal Network on VLBW infants (birth weight
1500 g) who were born in Israel from 1995 to 2003. All 28 neonatal departments in Israel are included in data collection, which comprises the Israel National VLBW Infant Database (see the acknowledgments). Data are prospectively collected on a prestructured form and include information on the parents; maternal pregnancy history; antenatal care; details of the delivery; the infant's status at delivery; diagnoses, procedures, and complications during hospital stay; and outcome at discharge. All liveborn infants in Israel receive a unique identification number at birth. Patient information that is received by the database coordinator is checked for missing items and logic errors, corrected, completed, and then entered into a computerized database. Patient information is cross-checked with the Israeli national birth registry, and data from any missing infants are requested from the birth hospital. Data are collected on all infants until discharge from the hospital or death. Data on additional infant deaths that occurred after discharge but before 1 year of age were provided by the Ministry of Health from the national linked birth and death certificates and incorporated into the VLBW database. This study was approved by the Helsinki committee of the Sheba Medical Center, Tel Hashomer.
Definitions
Definitions used were concordant with those of the Vermont Oxford Neonatal Database Manual of Operation.7 Gestational age (in completed weeks) was determined by the best obstetric estimate of gestational age on the basis of last menstrual period, obstetric history and examination, prenatal ultrasound, and postnatal physical examination. SGA was defined as birth weight >2 SD below the mean weight for gestational age, according to the intrauterine growth charts of Usher and Mclean.8 Maternal hypertensive disorder was defined as either chronic hypertension (persistent elevation of blood pressure before 20 weeks of gestation or before pregnancy) or pregnancy-induced hypertension if blood pressure of >145/95 was first recorded after 20 weeks of gestation. Antenatal steroid therapy was considered as either "no" treatment or "any" treatment, which included infants’ receiving partial or complete courses of therapy. The diagnosis of respiratory distress syndrome (RDS) was recorded in the presence of a chest radiograph consistent with RDS together with supplemental oxygen or mechanical ventilation treatment. Bronchopulmonary dysplasia (BPD) was defined as oxygen dependence at 36 weeks’ postmenstrual age.9 Patent ductus arteriosus (PDA) was diagnosed when a heart murmur compatible with PDA was detected and left-to-right shunting was shown by Doppler examination. In addition, 
2 of the following were required: bounding pulses, hyperdynamic precordium, radiographic evidence of cardiomegaly or pulmonary edema, and inability to decrease ventilator settings in the first 48 hours after birth. Late-onset sepsis was defined as positive microbial growth on 1 blood cultures obtained after 72 hours of life accompanied by clinical signs of sepsis. Necrotizing enterocolitis (NEC) was diagnosed by the presence of clinical and radiologic characteristics according to the criteria of Bell et al.10 Only definite NEC (Bell stages 2 and 3) was included. The presence of seizures was reported when noted clinically and electroencephalographic evidence of seizure activity was not required. The use of anticonvulsant therapy for the treatment of seizures was recorded. Intraventricular hemorrhage (IVH) was diagnosed by cranial ultrasonography conducted within the first 28 days of life and graded according to the classification of Papile et al.11 Cystic periventricular leukomalacia (PVL) was considered when multiple small periventricular cysts were present on cranial ultrasound examination. Periventricular echogenicity or porencephalic cysts in the area of previously identified intraparenchymal hemorrhage were not included.12
Statistical Analysis
Differences in the postdischarge IMR according to demographic and perinatal characteristics and neonatal morbidities were tested using the 
2 test for categorical variables. Multivariable logistic regression analyses were used to account for the following confounding variables: maternal age, maternal education, gestational age, birth weight, SGA, gender, ethnic origin, antenatal steroid therapy, maternal hypertensive disorders, delivery mode, Apgar score, multiple births, RDS, PDA, sepsis, NEC, grades 3 to 4 IVH, PVL, seizures, BPD, and congenital malformations. Results of the logistic regression are presented as odds ratios (ORs) and 95% confidence intervals (CIs). Statistical analyses were performed by using SAS 9.1 statistical software (SAS Institute, Inc, Cary, NC).
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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During the years 1995–2003, 13430 VLBW (
1500 g) infants were recorded in the Israel VLBW infant database, accounting for >99% of all liveborn VLBW infants in Israel. Of these, 2828 (21%) died before discharge from the hospital. Early neonatal deaths (0–6 days) occurred in 1875 infants (66.3% of hospital deaths), late neonatal deaths (7–27 days) in 568 infants (20.0% of hospital deaths), and in-hospital postneonatal deaths (>28 days) in 385 infants (13.6% of deaths). The remaining 10602 infants were discharged from the hospital and composed the study sample. Infant deaths after discharge from the hospital but before 1 year of age were reported in an additional 80 infants, representing a mortality rate of 7.5 per 1000 infant discharges or 5.9 per 1000 live births 1500 g. These deaths occurred at a median of 81 days after discharge (interquartile range: 34–145 days).
The postdischarge IMRs by demographic and perinatal characteristics are shown in Table 1. The mortality rates were markedly higher in non-Jewish infants (18.0 per 1000 discharges), in infants who were born to mothers <20 years of age (24.5 per 1000 discharges), and in infants who were born to mothers with <9 years of education (18.2 per 1000 discharges). A strong association between birth weight and postdischarge mortality was present (Table 2), decreasing from 14.7 per 1000 among infants who weighed <750 g to 5.5 per 1000 in those who weighed 1000 to 1249 g. The mortality was highest among infants of gestational age <26 weeks (17.5 per 1000) and 34 weeks (11.1 per 1000) compared with 8 per 1000 at 26 to 29 weeks and 5 per 1000 at 30 to 33 weeks. Infants with congenital malformations and those with reported seizures during their hospitalization had very high postdischarge mortalities (27.2 and 30.3 per 1000 discharges, respectively).
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Among infants with BPD, the postdischarge IMR was 23.0 per 1000 in infants who were discharged receiving home oxygen therapy and 22.5 per 1000 among those who were prescribed home monitors, as compared with 15.2 and 14.2 per 1000 (not significant) in infants without these treatment modalities, respectively. Infants who had neonatal seizures and were discharged with or without anticonvulsant therapy had similar postdischarge mortality rates, 30.0 and 32.8 per 1000, respectively.
Maternal age and maternal education were significantly correlated, and the pattern of postdischarge mortality by maternal age and education in the Jewish and non-Jewish groups differed, as shown in Table 3. Among non-Jewish infants, mortality was significantly associated with maternal age (P < .02), whereas in the Jewish group, it was significantly associated with maternal education (P < .001). On the basis of this bivariate analysis, variables that combined Jewish ethnicity and maternal education and combined non-Jewish ethnicity and maternal age were entered into the multivariate model.
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In a multivariable analysis (Table 4), we determined that the odds for death after discharge was higher among infants who were born to Jewish mothers with <9 years of education (OR: 3.9) and in non-Jewish mothers who were younger than 20 years (OR: 6.4) and 20 to 34 years of age (OR: 4.7), as compared with Jewish mothers with >8 years of education. Furthermore, postdischarge mortality was independently associated with congenital malformations (OR: 3.4), neonatal seizures (OR: 3.0), NEC (OR: 2.2) and BPD (OR: 2.4). Inclusion of BPD diagnosed on the basis of oxygen dependence at 28 days of age showed a similar effect (OR: 2.0; 95% CI: 1.0–4.0). Neither birth weight nor gestational age was significantly associated with postdischarge mortality, and there was no significant association with other perinatal or neonatal variables entered into the multivariable model, including multiple births, maternal hypertension, delivery mode, Apgar score, SGA, gender, RDS, PDA, sepsis, IVH, and PVL.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Our study found that the rate of postdischarge deaths for VLBW infants in Israel was relatively low, 7.5 per 1000 infants discharged from the hospital, and accounted for <3% of all VLBW infant deaths. Death rate was significantly higher in non-Jewish infants, in infants who were born to young mothers, and in infants who were born to low-educated mothers. Higher postdischarge mortality was also independently associated with the presence of congenital malformations, neonatal seizures, NEC, and BPD.
The relative low postdischarge mortality in our recent study is encouraging. Hulsey et al6 reported in a single center from South Carolina, for infants who were born between 1981 to 1986, postdischarge mortality rates of 12.6 per 1000 for low birth weight infants (<2500 g), 7.8 per 1000 for preterm infants (<37 weeks of gestational age), 11.0 per 1000 for NICU graduates, and 22.5 per 1000 for VLBW infants.
Our study is 1 of a few population-based studies to investigate postdischarge mortality in VLBW infants.13–15 Population-base studies in contrast to single institutions’ experience15–18 are larger and more representative, and their findings may be generalized. Two previous studies from the 1980s focused on center-specific mortality rates after NICU discharge, reporting a ninefold and sevenfold excess in postneonatal mortality among NICU graduates compared with non-NICU graduates.16,19 Allen et al15 in a state study from Georgia that assessed data from 1980 to 1982 reported a postdischarge mortality of 22.7 per 1000 NICU discharges, which was 5 times higher than the postneonatal mortality in the general population. Although the overall postneonatal mortality and postdischarge mortality rates are not entirely comparable, the study emphasized the vulnerability of infants who are discharged from the NICU. Kempe et al13 reported that 79% of the infants who were born at >500 g and died in the postneonatal period were discharged before death. Only 1.3% of the postdischarge deaths were prematurity-related, and of all postneonatal deaths, only 16% of infants left the hospital with an identified high-risk medical condition. In our study of VLBW infants, of the 2908 (21.6%) infants who died up to 1 year of age, postneonatal deaths (>28 days) in hospital occurred in 13.2%, and infant deaths after discharge occurred in only 2.8%. It is reassuring to the families that if the preterm infant survives the NICU course, then the risk for death after discharge seems to be relatively small.
In our study, death rate was significantly higher in non-Jewish infants and in infants who were born to young mothers or to mothers with low education levels. These findings are in accordance with previous studies that found that maternal characteristics have a significant impact on postneonatal infant mortality.1,3,13,14,17,20–22 Kempe et al13 reported that infants of black as compared with white mothers had higher risk for dying of all major causes of death in the postneonatal period. In ethnic-specific analysis of postneonatal death, older maternal age was associated with a decreased risk in Latina and white women.3 In all 3 ethnic groups, having <12 years of education was significantly associated with an increased risk for postneonatal mortality, and among white women, having >15 years of education was associated with decreased risk. Few investigators did not find a significant association between postdischarge mortality and mother's income, age, marital status, education, or ethnicity.6,15 Although not all studies are in agreement, it is not difficult to speculate that young mothers and less educated women may be less sophisticated in their child-caring abilities, have greater social stresses in their lives, and have less access to social and medical support.
In our study, after adjusting for ethnicity, maternal age, and education, postdischarge mortality was independently associated with congenital anomalies, neonatal seizures, NEC, and BPD. Piecuch et al23 found in a single-center study that only BPD and intracranial hemorrhage (ICH) were independently associated with postdischarge death, but ICH alone was the most worrisome risk factor associated with sudden unexpected death. None of the infants who died with ICH had had seizures or were on anticonvulsive therapy in his study. Convulsions in neonates are not regarded as epilepsy but may share physiologic consequences. Seizure activity can disrupt normal physiologic regulation and control of respiratory and cardiac activity, which could lead to sudden death or apparent life-threatening events.24,25 Stratton et al26 reported in the critical conditions associated with apparent life-threatening events seizures in 8% and ICH in 3%. Although infants with epilepsy have an increased risk for death, most deaths occurred in children with severe underlying neurologic conditions and were not directly related to the occurrence of seizures.27 This study and others28,29 indicate that mortality in children with seizures is only minimally, if at all, elevated in children who are neurologically normal. In our study, we did not find a difference in the postdischarge mortality rate regardless of whether seizures were treated with anticonvulsants at the time of discharge from the NICU.
Our study found that infants who had NEC were at a twofold higher risk for postdischarge death. Among low birth weight infants, >16% of deaths related to NEC occur after 28 days and before 1 year of age.30 Long-term follow-up of infants who required surgery for NEC showed that infants who could be discharged from their primary hospitalization had a >80% to 95% chance of long-term survival.31 In the study of Callaghan et al,2 only 7% of deaths that were attributable to preterm birth were postneonatal, and the leading causes, accounting for 60% of postneonatal deaths that were attributable to preterm birth, were BPD and gastrointestinal disorders.
Infants with BPD are at increased risk for long-term complications, including readmission to hospital, pulmonary hypertension, death, and SIDS.32–36 Only a few studies evaluated potential predictors for these adverse events, and most focused on hypoxemia and/or the need for supplemental oxygen.32,33,37 Piecuch et al23 found that moderate to severe BPD was associated with postdischarge death, but the incidence of sudden unexpected death was not significantly different from the incidence in infants with a history of minimal oxygen needs. This is in accordance with our findings that postdischarge infant mortality was not associated with oxygen or home monitor requirements at discharge. There is no support from other studies that apnea monitors are protective.38
In our study, we did not show a significant independent association of postdischarge mortality with perinatal or neonatal variables such as multiple births, delivery mode, SGA, gender, maternal hypertension, gestational age, birth weight, RDS, PDA, sepsis, PVL, or IVH. Piecuch et al23 similarly did not find association between death and factors such as birth weight, gestational age, growth retardation, and gender. In the single-center study of Hulsey et al,6 infants who were delivered preterm, infants who had low birth weight, and NICU graduates had a higher risk for postdischarge mortality. The OR for mortality among VLBW infants was 5.7, and these infants composed 14.8% of postdischarge deaths.
Information on the cause of death would undoubtedly complement the results of our study. Unfortunately, because of cultural and religious reasons, postmortem examinations are rarely performed in Israel, and information recorded on the death certificate is of limited use in determining the actual cause of death. Despite this limitation, we were able to identify a number of perinatal factors that were independently associated with an excess risk for postdischarge deaths. The question arises whether additional modifications of the environment, such as improved infant care and parenting techniques, closing social and ethnic gaps, or better treatment or monitoring of infants with BPD or seizures, might influence the outcome of these vulnerable infants.
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CONCLUSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Although the post discharge death rate was relatively low in our cohort of VLBW infants, attention should be focused to the subgroups of infants who are at higher risk to minimize deaths among VLBW infants who are discharged from the hospital from the NICU.
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ACKNOWLEDGMENTS |
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The Israel National VLBW infant database is supported partially by the Israel Center for Disease Control and the Ministry of Health.
Following are the Israel Neonatal Network, participating centers in the Israel National VLBW infant database. Coordinating center: Women and Children's Health Research Unit, Gertner Institute for Epidemiology and Health Policy Research, Tel Hashomer. Neonatal departments: Assaf Harofeh Medical Center, Rishon Le Zion; Barzilay Medical Center, Ashkelon; Bikur Holim Hospital, Jerusalem; Bnei Zion Medical Centre, Haifa; Carmel Medical Center, Haifa; English (Scottish) Hospital, Nazareth; French Hospital, Nazareth; Hadassah University Hospital Ein-Karem, Jerusalem; Hadassah University Hospital Har Hazofim, Jerusalem; Haemek Medical Center, Afula; Hillel Yafe Medical Center, Hadera; Italian Hospital, Nazareth; Kaplan Hospital, Rehovot; Laniado Hospital, Netanya; Maayanei Hayeshua Hospital, Bnei-Brak; Meir Medical Center, Kefar Saba; Misgav Ladach Hospital, Jerusalem; Naharia Hospital, Naharia; Poria Hospital, Tiberias; Rambam Medical Center, Haifa; Rivka Ziv Hospital, Zefat; Schneider Children's Medical Center of Israel and Rabin Medical Center (Beilinson Campus), Petach-Tikva; Shaare-Zedek Hospital, Jerusalem; Sheba Medical Center, Tel-Hashomer; Soroka Medical Center, Beer-Sheva; Sourasky Medical Center, Tel-Aviv; Wolfson Medical Center, Holon; Yoseftal Hospital, Eilat.
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FOOTNOTES |
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Accepted Feb 23, 2007.
Address correspondence to David Bader, MD, MHA, Department of Neonatology, Bnai Zion Medical Center, 47 Golomb St, Haifa 31048, Israel. E-mail: dramir{at}netvision.net.il
The authors have indicated they have no financial relationships relevant to this article to disclose.
Drs Kugelman and Reichman contributed equally to this study.
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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics
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