Original Article

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Influence of Perinatal Factors in Short- and LongTerm Outcomes of Infants Born at 23 Weeks of Gestation Hamzah R. Miltaha, MD1 Lisa M. Fahey, MD2 Jonathan K. Muraskas, MD1

Christine H. Sajous, MD1

1 Division of Neonatal Medicine, Department of Pediatrics, Loyola

University Medical Center, Maywood, Illinois 2 Department of Pediatrics, New York Presbyterian-Weill Cornell Medical Center, New York, New York 3 Division of Maternal Fetal Medicine, Department of Obstetrics and Gynecology, University of Mississippi Medical Center, Jackson, Mississippi

John C. Morrison, MD3

Address for correspondence Jonathan K. Muraskas, MD, Division of Neonatal Medicine, Department of Pediatrics, Loyola University Medical Center, 2160 S. 1st Avenue, Maywood, IL 60153 (e-mail: [email protected]).

Abstract

Keywords

► ► ► ►

neonatal outcome periviable birth risk factors survival

Objective Investigate the influence of perinatal factors on short- and long-term outcomes for infants born at 23 weeks of gestation. Study Design This is a retrospective study over a 25-year period (1987–2011) of 87 successfully resuscitated infants at 23 weeks of gestation. We investigated the effects of poor prenatal care, race, gender, chorioamnionitis, antenatal corticosteroids, delivery route/location, low 5-minute Apgar score, birth weight, and multiple births on shortand long-term outcomes. Results The mortality rate was 43% (37/87). A total of 88% (44/50) of the survivors were followed at 2 years corrected age with 66% (29/44) diagnosed with a moderate-tosevere neurological impairment. Outborn and multiple birth infants had significantly higher mortality (p-value 0.042 and 0.006, respectively). Lack of exposure to antenatal steroids and lower birth weight significantly increased the disability score (p-value 0.042 and 0.003, respectively). Conclusion Multiple perinatal factors significantly influence outcomes at the threshold of viability.

The survival of extremely low gestational age newborns (ELGAN, live births < 28 weeks of gestation) has improved considerably over the last three decades in the developed countries.1 Neonatologists routinely provide intensive care for infants born at 25 weeks of gestation. Before 23 weeks of gestation, 93% of neonatologists in the United States considered treatment futile due to extreme immaturity and low survival rates.2 Infants born at 24 weeks of gestation are still considered to be in a gray zone relative to resuscitation decisions.3 The survival of infants born between 230/7 and 236/7 weeks of gestation, which are termed fetal newborns (FNs),4 is considerably less. These survival rates show an

average increase over the last two decades, and range between 26 and 66%.5 Although, the prevalence of ELGAN is less than 1% of all live births, it accounts for nearly one-half of all the perinatal deaths. In addition, ELGAN births represent a disproportionate percentage of the nearly $26 billion spent annually in the United States on preterm births and their consequences.6 Despite the increasing survival of FNs, intact survival rates without severe or profound neurodevelopmental impairment (NDI) have not kept pace, and remain low at 20%.7 Short- and long-term outcomes of FN are increasingly reported, though they remain scattered and conflicting due

received May 30, 2014 accepted after revision July 25, 2014 published online December 8, 2014

Copyright © 2015 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.

DOI http://dx.doi.org/ 10.1055/s-0034-1390350. ISSN 0735-1631.

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Am J Perinatol 2015;32:627–632.

Perinatal Factors Influencing Outcomes of Fetal Newborns to considerable variability on the definitions of survival and different levels of NDI.8 A significant variable, for example, is whether to include delivery room deaths, even if no resuscitation efforts are made. FNs are often clinically stable in the first 24 to 48 hours of life, referred to as the “honeymoon period.” However, during the ensuing days, many of the FNs tend to become clinically unstable with significant morbidity and mortality related to intraventricular hemorrhage (IVH), infection, and cardiopulmonary problems often making it difficult to counsel parents regarding withdrawal/withholding treatment. Currently, there is no consensus on early treatment strategies that can accurately predict survival, severe morbidity or NDI based on observations in the first 48 hours of life.9 As a result, the uncertainties at this threshold of viability can cause medical and ethical dilemmas.10 Perinatal factors have been evaluated to predict survival or outcomes of FN. Antenatal corticosteroids are increasingly used after accumulative evidence of promoting fetal lung maturity or preventing NDI. Significant reduction in mortality and the frequency of grades 3 and 4 IVH has been demonstrated among infants born between 23 through 25 weeks of gestation. In 1993, less than 20% of infants born before 26 weeks of gestation had been exposed to antenatal corticosteroids, this percentage has increased to 60% among FNs.11 Some studies have suggested that delivery by cesarean section conveys advantages to survival among ELGAN, though the overall impact of cesarean section lacks consensus especially among FNs.12 A systematic review and meta-analysis has demonstrated that female sex, singleton birth, and delivery room resuscitation at a tertiary center significantly improves survival among ELGAN. Although this review has included FNs, the presence of other gestational ages has the potential to alter this conclusion. African American race has a significantly higher survival rates in many studies among ELGAN, but there is still conflicting evidence regarding the role of race/ethnicity on survival among FNs.13 Another study has demonstrated a higher survival among late FNs (234/7–236/7 weeks of gestation) when compared with FNs born earlier.14 Clinical chorioamnionitis increases the risk of early-onset sepsis and severe IVH among preterm infants.15 In addition, the infection stimulates fetal inflammatory response, and can accelerate the maturation of fetal lungs and brain.16 The opposing effects of chorioamnionitis make the clinical outcome unpredictable, especially on the FN group which has not been studied before. We hypothesize that certain obstetric and immediate postnatal markers may provide some protective effect on the FNs. If an association between certain perinatal factors and outcomes of the FN could be established, then the presence or absence of these particular perinatal factors may influence the decision to initiate aggressive management versus comfort care in these FNs.

Methods This study was performed at Loyola University Medical Center, in Maywood, IL and was approved by the Institutional American Journal of Perinatology

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Miltaha et al. Review Board (number: 202030). Over a 25-year period (1 January, 1987 through 31 December, 2011) we retrospectively evaluated our experience with the 87 FNs who met the inclusion criteria of being: (1) Inborn and outborn infants born between 230/7 and 236/7 weeks of gestation and (2) resuscitated and survived to be admitted to our neonatal intensive care unit (NICU). We identified the FNs from our admission records and reviewed the records of mothers and their offspring. The gestational age determination was based on the best obstetric estimate using menstrual dating and first or second trimester ultrasound. We identified certain perinatal factors that included poor prenatal care, non-African American maternal race, clinical chorioamnionitis, no antenatal corticosteroids, outborn birth, cesarean delivery, 5-minute Apgar score of < 7, and multiple births. We defined poor antenatal care by less than three total antenatal visits, or the first visit starting in the second trimester. Clinical chorioamnionitis was defined as meeting the following criteria: the presence of maternal fever ( 100.4°F for  1 hour), foul-smelling amniotic fluid, and sustained fetal tachycardia (> 160 beats/min for  1 hour). Antenatal corticosteroid use was defined if at least one dose of betamethasone was administered more than 12 hours before delivery to accelerate fetal lung maturity. FNs resuscitated at other hospitals before being transported to our NICU were classified as outborn. The mean gestational age and birth weight along with the median first three Apgar scores were calculated. Infants delivered at 230/7 to 233/7 weeks of gestation were grouped into early FNs and those at 234/7 to 236/7 weeks of gestation were considered late FNs. The primary short-term outcome was mortality during NICU stay. Secondary short-term outcomes were: total IVH, severe (grade 3 or 4) to total IVH, retinopathy of prematurity (ROP) requiring treatment among survivors, surgical closure of symptomatic patent ductus arteriosus (PDA), necrotizing enterocolitis (NEC) stage 2 or 3, culture proven sepsis, and NICU discharge on oxygen. IVH was reported and graded according to the classification of Papile et al.17 ROP treatment was by laser coagulation, cryocoagulation therapy, or both. Symptomatic PDA was defined based on both echocardiographic findings and clinical evidence of volume overload because of left-to-right shunting. Surgical closure of symptomatic PDA was by suture ligation or clip application, and was performed after failure of medical therapy with ibuprofen or indomethacin, or if medical therapy was contraindicated. NEC was defined according to the classification of Bell et al.18 Culture proven sepsis was defined as temperature instability or cardiopulmonary compromise along with positive blood culture. Surviving infants were followed in the neonatal developmental clinic up to 1 year corrected age,19 and in the developmental pediatric clinic afterward. The pediatrician and developmental therapist performed physical examinations and neurodevelopmental assessment at 3 to 6 month intervals using the current version of Bayley Scales of Infant Development.20 We reviewed records of the neonatal developmental clinic and the developmental pediatrician clinic up to 2 years corrected age. The

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Results Of the total 161 FNs noted throughout this study period, 74 were either unsuccessfully resuscitated or not resuscitated at all in the delivery room after discussion with parents before delivery. In many cases, the neonatology team was not asked to attend the delivery. Of the 87 FNs that were resuscitated and admitted to the NICU, the mean gestational age and birth weight were 234/7 weeks and 581 g, respectively. The median Apgar scores were 3, 6, and 7 at 1, 5, and 10 minutes, respectively. Out of the 87 FNs, 15% were outborn, 47% were delivered by cesarean section, 65% had an Apgar score of less than 7 at 5 minutes, and 17% were multiple births. Overall 16% of the mothers had poor prenatal care, 64% were not African Americans, 24% had clinical chorioamnionitis, and 61% had no antenatal corticosteroids. All the outborn infants were transferred from satellite intermediate units within hours of birth. The outcomes are presented in ►Table 1. Overall 37 of the 87 FNs studied (43%) expired; 16 (43%) expired before 14 days of life, 6 (16%) expired between 14 and 30 days, 15 (41%) expired after 30 days of life. The average length of stay until discharge for survivors was 130 days and the mean postmenstrual age at discharge for the survivors was 42 weeks and 1 day. Out of the 50 survivors, 44 (88%) were followed up in our clinics through 2 years corrected age, and were categorized into three disability scores (►Table 1). The perinatal factors were

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Table 1 Short and long-term outcomes of the FN Short-term outcome

Affected/n (%)

Mortality during NICU stay

37/87 (43)

Total IVH

55/81a (68)

Severe to total IVH

45/55 (82)

ROP treatment among survivors

13/50b (26)

Surgical closure of symptomatic PDA

31/71c (44)

NEC stage 2 or 3

8/87 (9)

Culture proven sepsis

37/82d (45)

NICU discharge on oxygen

34/50b (68)

Long-term outcome

n ¼ 44 (%)

Mild or no disability

15 (34)

Moderate disability

17 (39)

Severe disability

12 (27)

Abbreviations: FN, fetal newborns; IVH, intraventricular hemorrhage; NEC, necrotizing enterocolitis; NICU, neonatal intensive care unit; PDA, patent ductus arteriosus; ROP, retinopathy of prematurity. a Six FN expired before the first cranial ultrasound evaluation. b Fifty FN survived and were discharged from the NICU. c Sixteen FN did not fulfill the criteria of symptomatic PDA or expired before evaluation. d Five FN had missing blood culture data.

not significantly different among these three groups when compared using chi-square or Fisher exact test. Clinical chorioamnionitis was significantly higher in females (p-value: 0.021). Of the outcomes, NICU mortality and ROP treatment were significantly higher in males (p-values: 0.015 and 0.005, respectively). No significant differences between females and males were found in the other perinatal factors or outcomes. Multiple perinatal factors were significantly different between early and late FN groups. Clinical chorioamnionitis was higher in early FNs (p-value: 0.009). Non-African American maternal race, cesarean delivery, and multiple births were higher in late FNs (p-values: 0.034, 0.012, and 0.001, respectively). Surgical closure of symptomatic PDA was significantly higher in the early FN group (p-value: 0.038); on the other hand ROP treatment and proven sepsis were significantly higher in the late FN group (p-values: 0.016 and 0.037, respectively). ►Table 2 presents the statistically significant predictors of short and long-term outcomes. The perinatal factors, along with the birth weight were studied. Outborn and multiple birth, infants were significantly at higher risk for NICU mortality. The odds of severe IVH for infants exposed to clinical chorioamnionitis decreased 87% as compared with that for infants not exposed to this complication. When the variables were modeled against the odds of culture proven sepsis, four of the perinatal factors were significant. Late FNs, lack of exposure to antenatal corticosteroids, outborn birth, and vaginal delivery increased the odds of proven sepsis significantly. An increase of 1 g of birth weight above the mean for the cohort decreased the odds of discharge on American Journal of Perinatology

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physicians and therapists were not blinded to the perinatal history. We classified the long-term outcomes of each FN into one of three categories: severe, moderate, and mild or no disability. Severe disability was defined as hearing impairment, visual impairment, or nonambulatory cerebral palsy. Moderate disability was defined as ambulatory cerebral palsy or abnormal neurological examination findings not consistent with severe disability. Mild disability was defined as learning disability or poor motor coordination not consistent with severe or moderate disability. Hearing impairment was defined as when amplification was required, and visual impairment was defined as blindness or no functional vision in one or both the eyes. Cerebral palsy was defined as nonprogressive, nontransient central nervous system disorder characterized by abnormal muscle tone in at least one extremity and abnormal control of movement and posture. Statistical analysis was performed using chi-square or Fischer exact test to determine the association between these factors and outcomes, and to compare them based on infant’s gender and gestational age. Variables with a p-value of  0.05 were determined to be significant. To adjust survival and other short-term outcomes for our FNs cohort, a stepwise multivariable logistic regression analysis was performed for each short-term outcome, and the effects of birth weight and the perinatal factors were investigated. Long-term outcomes at 2 years corrected age were ordinally scaled, and a cumulative logit model was used to investigate the effects of the birth weight and the perinatal factors on receiving a higher disability score.

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Table 2 Multivariable logistic regression model of short- and long-term outcomes Outcome

Significant variable

Mortality during NICU stay Severe to total IVH ROP treatment among survivors

OR

CI

p-Value

Outborn

4.23

1.05–16.97

0.042

Multiple birth

7.56

1.80–31.71

0.006

Clinical chorioamnionitis

0.13

0.02–0.86

0.035

Male

12.85

2.16–76.56

0.005

Late FNa

7.11

1.17–43.34

0.034

Surgical closure of symptomatic PDA

Early FNb

3.66

1.10–12.35

0.035

Poor prenatal care

9.40

1.02–86.29

0.048

Culture proven sepsis

Late FN

11.67

2.43–56.15

0.002

No antenatal steroids

5.13

1.40–18.87

0.014

Outborn

14.26

2.11–96.48

0.007

Vaginal delivery

4.35

1.16–16.67

0.028

NICU discharge on oxygen

Higher birth weight (g)

0.98

0.96–1.00

0.020

Higher disability score

No antenatal steroids

4.65

1.06–20.41

0.042

Higher birth weight (g)

0.98

0.97–0.99

0.003

Abbreviations: CI, confidence interval; FN, fetal newborns; IVH, intraventricular hemorrhage; NICU, neonatal intensive care unit; OR, odds ratio; PDA, patent ductus arteriosus; ROP, retinopathy of prematurity. a Late FN, 234/7–236/7. b Early FN, 230/7–233/7.

oxygen by 2.2%. None of the variables were significant when analyzed for the odds of total IVH or NEC stage 2 or 3. The only significant predictors of receiving a higher disability score at 2 years corrected age were lack of exposure to antenatal corticosteroids and lower birth weight. The odds of higher disability score decreased 78% with antenatal corticosteroids exposure. For every 1 g increase of birth weight above the mean, odds of higher disability score decreased 1.6%.

Discussion Over this 25-year study period, the definition of viability has changed considerably and the limits of viability have continued to decrease. In our study, 57% of successfully resuscitated infants survived, however, 66% of survivors had a moderate or severe disability at 2 years corrected age. These rates were not the same in infants exposed to different perinatal factors. Males had a higher mortality during their NICU stay, but this difference was not significant after correcting for other factors. The presence of chorioamnionitis decreased the risk of severe IVH, but did not demonstrate a significant effect on disability score. In 2004, Hoekstra et al reported a survival rate of 66% among FNs between the years 1996 and 2000.21 Various reports, on the other hand, revealed lower survival rates (between 26 and 58%).22,23 In a prospective cohort study the resuscitation of 100 consecutive FNs resulted in 40% survival. Resuscitation efforts were attempted universally, and 10 delivery room deaths were included in this analysis. Male gender, 5-minute Apgar score > 5 and placental examination consistent with chorioamnionitis were significantly higher among survivors.24 American Journal of Perinatology

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There is no time in pregnancy when the window of 7 days will have as much impact as it will at 22 to 25 weeks of gestation.25 Our study has not demonstrated significant differences in survival between early and late FNs (window of 3–4 days) as a previous study has done. There were significant differences in multiple perinatal factors between the groups in our study, so controlling the perinatal factors is essential in future studies to determine the effect of this narrow window on survival and NDI in FNs. Unreliability of ultrasound at this gestational age as well as unrealistic parental demands often results in clinicians practicing defensive medicine when treatment strategies might be of no benefit. Numerous studies have shown that a FN’s clinical appearance in the delivery room does not predict outcome.26 Furthermore, many clinicians still use 500 g as the cutoff to initiate delivery room resuscitation without specific data to support this unwritten guideline. A particular strength of this study is the high follow-up rate (88% among survivors) at 2 years corrected age. Also, this study has corrected for numerous confounding perinatal factors plus the birth weight using stepwise multivariable logistic regression analysis. These corrections have allowed further understanding of this specific gestational age group and the uniqueness of FN. In addition, this study has demonstrated how certain perinatal factors (e.g., gender and race) are less significant in predicting mortality and disability at the threshold of viability. Finally, having the study in a single perinatal center has allowed for less variations in practice patterns, as well as more uniform counseling and management. There are several limitations to this study. First, the definition of survival is controversial. Some studies have included delivery room deaths in their outcomes, while others have

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2 Peerzada JM, Richardson DK, Burns JP. Delivery room decision-

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Clinical Perspective • Long-term outcomes of FN remain dismal despite the increasing survival. • Perinatal factors have significantly contributed to the short- and long-term outcomes at the limit of viability. • Stepwise multivariable logistic regression analysis has corrected for multiple perinatal factors and allowed further understanding of this specific gestational age group and its uniqueness. • Coordinated family counseling between the obstetric and neonatal teams is necessary for mutual understanding. Conflict of Interest The authors declare no conflict of interest.

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Acknowledgment The authors would like to thank Rong Guo, MS, for providing statistical analysis.

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References 1 Fanaroff AA, Hack M, Walsh MC. The NICHD neonatal research

network: changes in practice and outcomes during the first 15 years. Semin Perinatol 2003;27(4):281–287

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included all deaths up to 1 year corrected age. Such discrepancies have the potential to alter outcome rates and add to the difficulty in comparing our results to previous studies. There is no precise information about death after discharge from the NICU. A second limitation is the long duration of the study. Over a 25-year period, many interventions have been established and have proven to change the outcomes of FN. These outcomes have not been compared between different years or decades. Third, 16% of the mothers had poor prenatal care which has the potential to affect accurate dating due to the lack of early ultrasound examination. The fact that the mean birth weight of FN in the study was similar to the 50th percentile of estimated fetal weight (568 g) of a commonly used reference27 is reassuring. A fourth limitation is that Bayley Scales of Infant Development at 2 years of life has limited validity for predicting school age performance.28 Despite a survival rate of 57% among successfully resuscitated infants, long-term outcomes of FN remain dismal. The extended length of stay as well as the significant rates of disability can contribute to the emotional and financial burden of families and depletion of limited health care resources. Our data are consistent with the National Institute of Child Health and Human Development Neonatal Research Network. Based on our data, we do not recommend universal resuscitation of these FN. Rather; each case should be evaluated by the obstetric and neonatal teams before a reasoned discussion with the families explaining the current data, when possible.29 There are legal and ethical data to support conservative management of FN when their overall prognosis is universally grim.

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Miltaha et al. premature infants: a national study. Pediatrics 2010;125(4): 696–703 27 Hadlock FP, Harrist RB, Martinez-Poyer J. In utero analysis of fetal growth: a sonographic weight standard. Radiology 1991;181(1): 129–133 28 Hack M, Taylor HG, Drotar D, et al. Poor predictive validity of the Bayley Scales of Infant Development for cognitive function of extremely low birth weight children at school age. Pediatrics 2005;116(2):333–341 29 Raju TNK, Mercer BM, Burchfield DJ, Joseph GF. Periviable birth: executive summary of a Joint Workshop by the Eunice Kennedy Shriver National Institute of Child Health and Human Development, Society for Maternal-Fetal Medicine, American Academy of Pediatrics, and American College of Obstetricians and Gynecologists. J Perinatol 2014;34(5):333–342

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Influence of perinatal factors in short- and long-term outcomes of infants born at 23 weeks of gestation.

Investigate the influence of perinatal factors on short- and long-term outcomes for infants born at 23 weeks of gestation...
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