Early Human Development 90 (2014) 113–118
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
The impact of cesarean section on neonatal outcome of infants born at 23 weeks of gestation Seishi Furukawa ⁎, Hiroshi Sameshima 1, Tsuyomu Ikenoue 1 Department of Obstetrics & Gynecology, Faculty of Medicine, University of Miyazaki, 5200 Kihara-Kiyotake, Miyazaki 889-1692, Japan
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Article history: Received 14 February 2013 Received in revised form 10 December 2013 Accepted 24 December 2013 Keywords: Premature infant 23 weeks Obstetrical indication Cesarean section
a b s t r a c t Objective: Determine the impact of cesarean section (CS) on neonatal outcome of infants born at 23 weeks of gestation. Methods: A retrospective study was performed involving 34 infants born at 23 weeks and 91 infants born at 24– 26 weeks. Indications necessitating delivery were severe pregnancy induced hypertension, non-reassuring fetal heart rate patterns (NRFHRs), or intrauterine infection (IUI). Obstetrical indication for CS included NRFHR and breech presentation. Poor outcome included neonatal death or cerebral palsy. Univariate and multiple logistic analyses were performed to determine the effect of CS for obstetrical indications on poor outcome. Results: The incidence of poor outcome was significantly higher at 23 weeks (number of poor outcomes/total number: 22/34) compared to that (31/91) at 24–26 weeks (p b 0.01). The incidence of a poor outcome was significantly higher at 23 weeks for infants having NRFHR (11/16) compared to those at 24–26 weeks (15/43, p = 0.02). However, the incidence of a poor outcome was similar in infants with IUI (6/10 at 23 weeks versus 5/11 at 24–26 weeks, p = 0.41). Vaginal birth in cases of obstetrical indication for CS at 23 weeks was associated with higher risk of a poor outcome (odds ratio: 8.2). In contrast, the risk at 24–26 weeks was not higher (OR, 0.8). After adjustment using variables of vaginal birth and IUI, vaginal birth significantly affected poor outcome (OR, 13.0). Conclusion: Poor neonatal outcome was closely related to the mode of delivery, suggesting that CS for obstetrical indication at 23 weeks may improve neonatal outcome. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Advances in perinatal medicine have reduced perinatal mortality and morbidity dramatically over the past 20 years [1–3]. However, the mortality of infants born at 22 and 23 weeks of gestation is still high. Infants currently born at 24–26 weeks of gestation can survive with aggressive prenatal and postnatal therapies. Due to the high mortality rate, infants born at 22–23 weeks of gestation are usually not the result of a cesarean section (CS). Obstetricians are therefore faced with a dilemma that requires a decision at the peri-viable period. However, there is presently limited information regarding how we can improve neonatal outcome of extreme prematurity. We previously reported a regional perinatal outcome of extremely low-birth weight infants (b1000 g) and showed an overall mortality rate of 9.2% [4]. In that study, we found that the mortality of infants born by cesarean section was significantly lower than that of infants born vaginally (9.8% vs. 28.8%, p b 0.05), suggesting that cesarean section is a good practice for extremely premature infants in order to improve neonatal outcome. The mortality rate of infants born at ⁎ Corresponding author. Tel.: +81 985 85 0988; fax: +81 985 85 6149. E-mail address: [email protected] (S. Furukawa). 1 Tel.: +81 985 85 0988; fax: +81 985 85 6149. 0378-3782/$ – see front matter © 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.earlhumdev.2013.12.010
23 weeks of gestation in our institute was relatively low (21.7%) [4], which prompted us to decrease the lower limit of CS for fetal indication to 23 weeks of gestation. Under the present circumstances, CS is provided in cases involving premature infants at 24 weeks or more. It was provided at 23 weeks only with parental agreement after counseling. The current study was conducted in the setting of a tertiary perinatal center. We firstly reviewed the medical records for coexisting perinatal factors that may contribute to poor outcomes and compared the deteriorating factors of infants born at 23 weeks and 24–26 weeks of gestation. Secondly, we evaluated the impact of CS for obstetrical indications on neonatal outcome of infants born at 23 weeks of gestation. 2. Materials and methods This study was undertaken retrospectively and there was therefore no need to obtain approval from a suitably constituted Ethics Committee in our institution. We retrospectively reviewed the medical charts of infants born at 23–26 weeks of gestation and admitted to the Perinatal Center, University of Miyazaki, from January 2000 to April 2010. Our center is the only tertiary perinatal center in the Miyazaki province of Japan. We have 11,000 births per year in the Miyazaki province and our neonatal center mainly deals with referral cases and premature infants with a birth weight of less than 1000 g. The infants were divided
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into two groups: 23 weeks of gestation and 24–26 weeks of gestation. Excluded from the study were cases involving multifetal pregnancy, fetal anomaly, and chromosomal abnormality. Gestational age was assessed on the basis of the last menstrual period and first-trimester ultrasound fetometry. The following clinical characteristics were collected: maternal age, premature rupture of the membranes (ROM), placental abruption (Abruption), intrauterine growth restriction (IUGR), parental refusal of CS for obstetrical indication, cesarean delivery, breech delivery, non-reassuring fetal heart rate pattern (NRFHR), intrauterine infection, severe preeclampsia, and puerperal infection including endometritis, sepsis, wound infection, and abscess formation in the pelvic cavity. The following neonatal characteristics were also collected: sex, birth weight (g), intraventricular hemorrhage (IVH) ≥ Grade 3, neonatal death (ND), and cerebral palsy (CP). Poor neonatal outcome included CP or ND. Fetal heart rate patterns were classified according to the NICHD guideline [5]. Cases of variable decelerations (VDs) were classified into mild, moderate (mVD), and severe (sVD) using Kubli's classification [6]. In this study, NRFHRs necessitating the termination of pregnancy included recurrent late deceleration, recurrent mVD, recurrent sVD, prolonged deceleration, or bradycardia. Placental abruption was defined by the presence of retroplacental hematoma and clinical presentations (any one or combination of genital bleeding, abdominal pain, pregnancy-induced hypertension, premature labor, ROM, intrauterine fetal death, or NRFHR) [7]. IUGR was defined as a sex-specific birth weight less than the 10th percentile for gestational age according to the Japanese standard growth curve for singletons [8]. Intrauterine infection was defined according to whether the presence of bacteria in amniotic fluid was determined by amniocentesis or clinical chorioamnionitis. Clinical chorioamnionitis was defined as the presence of a maternal febrile condition (N 38 °C), maternal tachycardia (N 120 beats/min), maternal leukocytosis (N15,000 cells/mm3), and an elevated CRP level (N5.0 mg/dl). Severe preeclampsia was defined as a case involving a severe condition, such as persistent severe hypertension (blood pressure ≥ 160/110 mm Hg), oliguria (b 500 ml/day), low platelet count (b 100,000/mm3), HELLP syndrome (hemolysis, elevated
liver enzyme, and low platelets), pulmonary edema or eclampsia. Severity of proteinuria was not an indication to terminate pregnancy. Neurodevelopmental assessment of a child with cerebral palsy was performed by independent pediatric neurologists that were blinded to the study. Assessment was performed at an age of 1 year or older. Infants with intracranial abnormalities including periventricular leukomalacia or IVH (≥ Grade 3) by MRI or cranial ultrasound were also categorized in the CP group in this study. The grading of IVH follows that described by Papile et al. [9]. Perinatal management along with fetal indications for 24–26 weeks is shown in Fig. 1. Fetal indications to terminate pregnancy were the presence of NRFHRs and intrauterine infection. NRFHRs were determined either at admission or following (intrapartum) FHR monitoring. Maternal indication was severe preeclampsia. Obstetrical indication for CS was either NRFHRs or breech presentation. If fetal and maternal indications to terminate pregnancy were present, we tried vaginal delivery with oxytocin for labor induction unless obstetrical indications for CS existed. We also provided aggressive neonatal resuscitation to all live births. These perinatal cares were given with parental consent. In contrast, CS was not recommended at 23 weeks of gestation; however, we provided it following a parental request after offering an informed choice between vaginal and cesarean birth for obstetrical indications. Moreover, antenatal corticosteroid treatment for mothers with preterm labor prior to 24 weeks was not routinely given at our institution. All neonates born at 23 weeks of gestation were fully resuscitated and cared by neonatologists [10,11]. We first compared clinical characteristics such as the incidence of ROM, Abruption, IUGR, NRFHRs, intrauterine infection, severe preeclampsia, parental refusal of CS for obstetrical indication, breech delivery, CS delivery, and puerperal infection between 23 weeks and 24–26 weeks. Cases of intrauterine infection followed by NRFHRs were categorized as intrauterine infection. The incidence of poor outcome including cerebral palsy and neonatal death was also compared between 23 weeks and 24–26 weeks. Patients were then divided into 3 groups comprising NRFHRs, intrauterine infection, and ‘other’ (in labor) according to the presence of fetal
Admission FHR monitoring Reassuring
NRFHRs
R/O IUI Absent
In labor
Present
Labor induction
CS Delivery
Breech (Intrapartum) FHR monitoring NRFHRs Fig. 1. Perinatal management for 24–26 weeks. IUI: intrauterine infection. NRFHR: non-reassuring fetal heart rate pattern.
S. Furukawa et al. / Early Human Development 90 (2014) 113–118
indications to terminate pregnancy. The incidence of indications based on poor outcome was compared between 23 weeks and 24–26 weeks. Finally, in order to elucidate the effect of CS for obstetrical indication on neonatal outcome, we categorized each case as either a cesarean or vaginal birth when obstetrical indications were present. At this time, cases of intrauterine infection followed by NRFHR or intrauterine infection with breech presentation were also candidates for CS. Univariate analysis was first performed to determine the effect of CS for obstetrical indication on poor outcome at the respective weeks of gestation. We considered the effect of co-existing deteriorating factors on neonatal outcome except for obstetrical indication, and multiple logistic analysis was then performed using dichotomous variables. Data are expressed as number, incidence (%), mean ± SD, or range. Comparisons between groups were made using the Student's t-test or χ2 tests. Probability values b0.05 were considered significant.
3. Results At 23 weeks, the CS rate was 47% (16/34) and was significantly lower than 70% (64/91) at 24–26 weeks (p = 0.01). There was no significant difference between groups concerning maternal age, ROM, Abruption, IUGR, breech delivery, puerperal infection, or NRFHRs (Table 1). There were no cases of severe eclampsia at 23 weeks. The incidences of intrauterine infection (p = 0.02) and parental refusal of CS for obstetrical indication (p b 0.01) were significantly higher at 23 weeks than those at 24–26 weeks. The incidence of poor outcome was significantly higher at 23 weeks (65%) than at 24–26 weeks (34%, p b 0.01, Table 2). Sixteen cases of NRFHR were found at 23 weeks. Two cases were detected on admission following FHR monitoring. Among the 16 cases, 4 were CP and 7 were ND. On the other hand, 43 cases of NRFHRs were found at 24–26 weeks. Ten cases were detected on admission following FHR monitoring. Among the 43 cases, 12 were CP and 3 were ND. The incidence of a poor outcome was significantly higher at 23 weeks (p = 0.02) (Fig. 2A). Ten cases of intrauterine infection were found at 23 weeks, among which 4 were CP and 2 were ND. On the other hand, 11 cases of intrauterine infections were found at 24–26 weeks and included 4 cases of CP and one case of ND. There was no significant difference concerning the incidence of a poor outcome between groups (p = 0.50, Fig. 2B). Eight cases of the ‘other’ group were found in the 23-week group, among which 5 were CP. On the other hand, 26 cases were categorized as ‘other’ for the 24–26week group, among which 5 were CP and 3 were ND. There was no significant difference concerning the incidence of a poor outcome between groups (p = 0.11). Table 1 Maternal characteristics associated with infants born at 23 and 24–26 weeks of gestation. Results are expressed as number, mean ± SD, or incidence (%). Comparisons were made using the Student's t-test or χ2 tests. ROM: rupture of membrane; Abruption: placental abruption; IUGR: intrauterine growth restriction; NRFHR: non-reassuring fetal heart rate pattern; CS: cesarean section. Gestational age at birth Number
23 34
24–26 91
p
Maternal age (yr) ROM (%) Abruption (%) IUGR (%) NRFHR (%) Intrauterine infection (%) Severe preeclampsia (%) Refusal of CS for obstetrical indication (%) Breech delivery (%) CS delivery (%) Puerperal infection
28.7 ± 5.5 19 (56) 9 (26) 2 (6) 16 (47) 10 (29) 0 (0) 10 (29) 8 (24) 16 (47) 4 (12)
30.1 ± 5.3 37 (41) 20 (22) 15 (16) 43 (47) 11 (12) 11 (12) 4 (4) 11 (12) 64 (70) 6 (7)
0.20 0.13 0.60 0.35 0.98 0.02 0.08 b0.01 0.10 0.01 0.27
ROM: rupture of membrane, Abruption: placental abruption, IUGR: intrauterine growth restriction, NRFHR: non-reassuring fetal heart rate pattern, CS: cesarean section.
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Table 2 Demographic data of infants at 23 and 24–26 weeks of gestation. Gestational age at birth Number
23 34
24–26 91
p
Sex; girl (%) Weight (g, mean ± SD) IVH ≥ Grade III (%) Poor outcome (%) Cerebral palsy Neonatal death
12 (35) 577 ± 82 12 (35) 22 (65) 13 9
49 (54) 700 ± 123 8 (9) 31 (34) 23 8
0.06 b0.01 b0.01 b0.01
IVH: intraventricular hemorrhage.
We categorized each case as either a cesarean or vaginal birth when obstetrical indications were present at 23 weeks (Fig. 3). Five cases without obstetrical indications for CS resulted in a vaginal birth. Among women who presented obstetrical indications for CS with or without parental refusal at 23 weeks (n = 29), 16 cases involved a cesarean birth (n = 13) and the others resulted in a vaginal birth (n = 16). Then, cases that involved those who underwent vaginal birth with obstetrical indications (n=16) were defined as poor management. While, cases that involved a cesarean or vaginal birth without obstetrical indications (n = 18) were defined as normal management. The incidence of a poor outcome was compared between these two management groups. Eight infants in the normal management group had a poor outcome, while 14 infants in the poor management group exhibited a poor outcome. When the delivery was not managed according to the obstetrical indication for CS (poor management) at 23 weeks, there was an 8-fold higher risk of a poor outcome (odds ratio: 8.2; 95% confidence interval: 1.3–51.4; p = 0.03). In contrast, a vaginal birth in cases of obstetrical indication for CS at 24–26 weeks did not increase the risk of a poor outcome (odds ratio: 0.8; 95% confidence interval: 0.2–3.5; p = 0.75). As intrauterine infections were frequently seen at 23 weeks, we performed multiple logistic analysis after adjusting for intrauterine infection and vaginal birth on neonatal outcome. Vaginal birth in cases of obstetrical indication for CS more significantly affected poor outcome at 23 weeks (odds ratio: 13.0; 95% confidence interval: 1.3–129.6; p =0.03). Intrauterine infection did not affect poor neonatal outcome at 23 weeks (odds ratio: 0.3; 95% confidence interval: 0.03–4.3; p = 0.33). 4. Discussion We showed that poor neonatal outcome at 23 weeks of gestation was closely related to vaginal birth in cases of obstetrical indication. When obstetrical indication for CS existed at 23 weeks, a vaginal birth was associated with a 13-fold increased risk of a poor outcome compared to cases involving a CS birth. The incidence of a poor neonatal outcome was significantly higher in the NRFHR group at 23 weeks than at 24–26 weeks, although the incidence of NRFHRs was similar. It is worth noting that parental refusal of CS for fetal indication was higher at 23 weeks (p b 0.01). Intrauterine infection was frequently observed at 23 weeks, which is consistent with our previous reports that inflammation is an important prognostic factor in extremely premature infants ≤25 weeks of gestation [12,13]. In this study, there was no difference in the incidence of intrauterine infection-related poor outcome between 23 weeks and 24–26 weeks, except for CS indication. In addition, we showed that intrauterine infection was not an independent factor that deteriorated neonatal outcome at 23 weeks in spite of the high incidence of intrauterine infection. Some recent reports indicate that intrauterine infection is not an independent risk factor for poor prognosis in premature infants [14–16]. These conflicting reports may suggest that intrauterine infection does not have a direct causal relationship with poor outcome in extremely premature infants. The effect of intrauterine infection on neonatal prognosis may be augmented by the presence of other risk factors such as gestational age, IUGR or birth asphyxia, as we previously
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A) NRFHR
B) Intrauterine Infection
p=0.02
p=0.50
100%
100%
90%
90%
80%
80%
70%
70%
60%
60%
50%
50%
40%
40%
30%
30%
20%
20%
10%
10%
0%
Poor outcome
0% 23
24-26
23
24-26
Gestational age at birth (weeks) Fig. 2. A. Comparison of NRFHR-related poor outcome between 23 weeks and 24–26 weeks. Poor outcome included cerebral palsy and neonatal death. NRFHR: non-reassuring fetal heart rate pattern. B. Comparison of intrauterine infection-related poor outcome between 23 weeks and 24–26 weeks. Poor neonatal outcome included cerebral palsy and neonatal death.
reported [13]. There is no difference in the management strategy for intrauterine infection from 23 to 26 weeks in this study. Our uniform management strategy in cases of intrauterine infection may also involve decreasing the association with worsening prognosis. On the other hand, the incidence of poor neonatal outcome was significantly higher in the NRFHR group at 23 weeks than at 24–26 weeks. There was a difference in the management strategy for NRFHR between 23 weeks and 24–26 weeks in the present study. However, all neonates born at 23–26 weeks of gestation were equally resuscitated [10,11]. Thus, obstetrical management greatly impacted neonatal outcome when involving NRFHR at 23 weeks. Cesarean delivery during the peri-viable period may reduce hemodynamic stress during labor. We have reported that intrapartum severe variable deceleration is associated with subsequent intestinal perforation in extremely premature infants [10]. We speculated that preventing prolonged periods of hazardous decelerations could reduce peripheral tissue hypoxia and prevent subsequent intestinal perforation. We have also shown that in poor-outcome infants born at 22–24 weeks of gestation, the catecholamine and volume load increased significantly to maintain adequate blood pressure and urination [11]. Thus, vaginal delivery during the peri-viable period induced hazardous NRFHRs and potentially affected cardiovascular stability. However, the beneficial effect of cesarean delivery during the peri-viable period is controversial [17]. One of the reasons for the inconsistent results is that the study population includes unadjusted co-existing factors such as intrauterine infection, IUGR, parental refusal, and the attitude of the physician. According to our results, vaginal birth in cases of obstetrical indication for CS did not affect neonatal outcome at 24–26 weeks, but produced an effect at 23 weeks. In Sweden, two different regional strategies for perinatal management of extreme prematurity co-existed, and indicated that CS for obstetrical indication was associated with improved neonatal outcome from 22 to 25 weeks without increased morbidity [18]. Due to the difficulty of conducting a controlled study, a comparison of different strategies within a homogenous group or comparison of different regional strategies is the only feasible method to prove the effectiveness of CS for obstetrical indication. Both studies support CS for obstetrical indication in extreme prematurity, particular at 23 weeks of gestation. Maternal complication associated with CS during the peri-viable period is an important matter for future pregnancies. A report from
the Cochrane Database indicated there was a significant advantage for women to undergo a preterm vaginal delivery compared to a preterm CS delivery with respect to maternal infection [17]. In our study, four cases of puerperal infection were found at 23 weeks, and three of the four cases involved CS. Likewise, six cases of puerperal infection were found at 24–26 weeks, and all involved CS. Obviously, the incidence of puerperal infection was high for cesarean section. Puerperal infection is one of the causes of infertility. Another concern for preterm CS is the potential risk of uterine rupture in the next pregnancy. We previously reported subsequent pregnancy outcomes (n = 103) in cases involving a vertical uterine incision for premature birth [19]. In this series, 33% (34/103) of patients were pregnant and the incidence of uterine rupture was 0% (0/32). Due to the small number of cases in that study, it is difficult to determine whether there is low risk of uterine rupture in subsequent pregnancy. Currently, there is no advantage for maternal health in preterm CS delivery. It is important to note that this study has some limitations. First, the current study involved only one tertiary hospital. Second, we did not consider the effect of steroid administration. Antenatal corticosteroid treatment before 24 weeks of gestation has been shown to improve neonatal outcome [20,21]. We did not routinely use antenatal corticosteroid treatment before 24 weeks; however, all neonates born at 22– 24 weeks received surfactant replacement therapy and hydrocortisone for circulatory stabilization [10,11]. The outcomes of neonates should be documented to verify the effect of antenatal corticosteroid treatment for extreme prematurity in future pregnancies. Third, we did not include the effect of parental refusal as a co-existing deteriorating factor on neonatal outcome. We focused on cases involving those who underwent vaginal birth with obstetrical indications for CS with or without parental refusal. In conclusion, we demonstrated that vaginal birth in cases of obstetrical indication for CS at 23 weeks resulted in a 13-fold higher risk of a poor outcome. Our results imply that neonates at 23 weeks would receive some benefit from a CS for obstetrical indication, compared with a vaginal birth.
Conflict of interest There is no relationship that might lead to a conflict of interest.
S. Furukawa et al. / Early Human Development 90 (2014) 113–118
117
Admission FHR monitoring Reassuring
NRFHR : 2
R/O IUI
Without IUI : 22
Vaginal birth
1 (Intrapartum) FHR monitoring
6
3
In labor Breech : 6 NRFHR : 7 NRFHR+Breech : 7 Reassuring: 2
POOR MANAGEMENT GROUP Reassuring R/O IUI
With IUI : 10 Vaginal birth
Labor induction: 9
1
In labor: 1
(Intrapartum) FHR monitoring
2
3
Breech : 1 NRFHR : 3 NRFHR+Breech : 3 Reassuring: 3
Fig. 3. Consequence of delivery in relation to obstetrical indication for cesarean section at 23 weeks. Upper part: cases with NRFHRs on admission and cases without IUI. Lower part: cases with IUI. IUI: intrauterine infection.
Acknowledgment This work was supported in part by a grant from the JAOG Ogyaa Donation Foundation and a grant (#79-258) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Parts of this study were presented as an oral presentation at The 47th Symposium of the Japan Society of Perinatal and Neonatal Medicine in Sapporo, Japan, 2011.
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
The impact of cesarean section on neonatal outcome of infants born at 23 weeks of gestation Seishi Furukawa ⁎, Hiroshi Sameshima 1, Tsuyomu Ikenoue 1 Department of Obstetrics & Gynecology, Faculty of Medicine, University of Miyazaki, 5200 Kihara-Kiyotake, Miyazaki 889-1692, Japan
a r t i c l e
i n f o
Article history: Received 14 February 2013 Received in revised form 10 December 2013 Accepted 24 December 2013 Keywords: Premature infant 23 weeks Obstetrical indication Cesarean section
a b s t r a c t Objective: Determine the impact of cesarean section (CS) on neonatal outcome of infants born at 23 weeks of gestation. Methods: A retrospective study was performed involving 34 infants born at 23 weeks and 91 infants born at 24– 26 weeks. Indications necessitating delivery were severe pregnancy induced hypertension, non-reassuring fetal heart rate patterns (NRFHRs), or intrauterine infection (IUI). Obstetrical indication for CS included NRFHR and breech presentation. Poor outcome included neonatal death or cerebral palsy. Univariate and multiple logistic analyses were performed to determine the effect of CS for obstetrical indications on poor outcome. Results: The incidence of poor outcome was significantly higher at 23 weeks (number of poor outcomes/total number: 22/34) compared to that (31/91) at 24–26 weeks (p b 0.01). The incidence of a poor outcome was significantly higher at 23 weeks for infants having NRFHR (11/16) compared to those at 24–26 weeks (15/43, p = 0.02). However, the incidence of a poor outcome was similar in infants with IUI (6/10 at 23 weeks versus 5/11 at 24–26 weeks, p = 0.41). Vaginal birth in cases of obstetrical indication for CS at 23 weeks was associated with higher risk of a poor outcome (odds ratio: 8.2). In contrast, the risk at 24–26 weeks was not higher (OR, 0.8). After adjustment using variables of vaginal birth and IUI, vaginal birth significantly affected poor outcome (OR, 13.0). Conclusion: Poor neonatal outcome was closely related to the mode of delivery, suggesting that CS for obstetrical indication at 23 weeks may improve neonatal outcome. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Advances in perinatal medicine have reduced perinatal mortality and morbidity dramatically over the past 20 years [1–3]. However, the mortality of infants born at 22 and 23 weeks of gestation is still high. Infants currently born at 24–26 weeks of gestation can survive with aggressive prenatal and postnatal therapies. Due to the high mortality rate, infants born at 22–23 weeks of gestation are usually not the result of a cesarean section (CS). Obstetricians are therefore faced with a dilemma that requires a decision at the peri-viable period. However, there is presently limited information regarding how we can improve neonatal outcome of extreme prematurity. We previously reported a regional perinatal outcome of extremely low-birth weight infants (b1000 g) and showed an overall mortality rate of 9.2% [4]. In that study, we found that the mortality of infants born by cesarean section was significantly lower than that of infants born vaginally (9.8% vs. 28.8%, p b 0.05), suggesting that cesarean section is a good practice for extremely premature infants in order to improve neonatal outcome. The mortality rate of infants born at ⁎ Corresponding author. Tel.: +81 985 85 0988; fax: +81 985 85 6149. E-mail address: [email protected] (S. Furukawa). 1 Tel.: +81 985 85 0988; fax: +81 985 85 6149. 0378-3782/$ – see front matter © 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.earlhumdev.2013.12.010
23 weeks of gestation in our institute was relatively low (21.7%) [4], which prompted us to decrease the lower limit of CS for fetal indication to 23 weeks of gestation. Under the present circumstances, CS is provided in cases involving premature infants at 24 weeks or more. It was provided at 23 weeks only with parental agreement after counseling. The current study was conducted in the setting of a tertiary perinatal center. We firstly reviewed the medical records for coexisting perinatal factors that may contribute to poor outcomes and compared the deteriorating factors of infants born at 23 weeks and 24–26 weeks of gestation. Secondly, we evaluated the impact of CS for obstetrical indications on neonatal outcome of infants born at 23 weeks of gestation. 2. Materials and methods This study was undertaken retrospectively and there was therefore no need to obtain approval from a suitably constituted Ethics Committee in our institution. We retrospectively reviewed the medical charts of infants born at 23–26 weeks of gestation and admitted to the Perinatal Center, University of Miyazaki, from January 2000 to April 2010. Our center is the only tertiary perinatal center in the Miyazaki province of Japan. We have 11,000 births per year in the Miyazaki province and our neonatal center mainly deals with referral cases and premature infants with a birth weight of less than 1000 g. The infants were divided
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into two groups: 23 weeks of gestation and 24–26 weeks of gestation. Excluded from the study were cases involving multifetal pregnancy, fetal anomaly, and chromosomal abnormality. Gestational age was assessed on the basis of the last menstrual period and first-trimester ultrasound fetometry. The following clinical characteristics were collected: maternal age, premature rupture of the membranes (ROM), placental abruption (Abruption), intrauterine growth restriction (IUGR), parental refusal of CS for obstetrical indication, cesarean delivery, breech delivery, non-reassuring fetal heart rate pattern (NRFHR), intrauterine infection, severe preeclampsia, and puerperal infection including endometritis, sepsis, wound infection, and abscess formation in the pelvic cavity. The following neonatal characteristics were also collected: sex, birth weight (g), intraventricular hemorrhage (IVH) ≥ Grade 3, neonatal death (ND), and cerebral palsy (CP). Poor neonatal outcome included CP or ND. Fetal heart rate patterns were classified according to the NICHD guideline [5]. Cases of variable decelerations (VDs) were classified into mild, moderate (mVD), and severe (sVD) using Kubli's classification [6]. In this study, NRFHRs necessitating the termination of pregnancy included recurrent late deceleration, recurrent mVD, recurrent sVD, prolonged deceleration, or bradycardia. Placental abruption was defined by the presence of retroplacental hematoma and clinical presentations (any one or combination of genital bleeding, abdominal pain, pregnancy-induced hypertension, premature labor, ROM, intrauterine fetal death, or NRFHR) [7]. IUGR was defined as a sex-specific birth weight less than the 10th percentile for gestational age according to the Japanese standard growth curve for singletons [8]. Intrauterine infection was defined according to whether the presence of bacteria in amniotic fluid was determined by amniocentesis or clinical chorioamnionitis. Clinical chorioamnionitis was defined as the presence of a maternal febrile condition (N 38 °C), maternal tachycardia (N 120 beats/min), maternal leukocytosis (N15,000 cells/mm3), and an elevated CRP level (N5.0 mg/dl). Severe preeclampsia was defined as a case involving a severe condition, such as persistent severe hypertension (blood pressure ≥ 160/110 mm Hg), oliguria (b 500 ml/day), low platelet count (b 100,000/mm3), HELLP syndrome (hemolysis, elevated
liver enzyme, and low platelets), pulmonary edema or eclampsia. Severity of proteinuria was not an indication to terminate pregnancy. Neurodevelopmental assessment of a child with cerebral palsy was performed by independent pediatric neurologists that were blinded to the study. Assessment was performed at an age of 1 year or older. Infants with intracranial abnormalities including periventricular leukomalacia or IVH (≥ Grade 3) by MRI or cranial ultrasound were also categorized in the CP group in this study. The grading of IVH follows that described by Papile et al. [9]. Perinatal management along with fetal indications for 24–26 weeks is shown in Fig. 1. Fetal indications to terminate pregnancy were the presence of NRFHRs and intrauterine infection. NRFHRs were determined either at admission or following (intrapartum) FHR monitoring. Maternal indication was severe preeclampsia. Obstetrical indication for CS was either NRFHRs or breech presentation. If fetal and maternal indications to terminate pregnancy were present, we tried vaginal delivery with oxytocin for labor induction unless obstetrical indications for CS existed. We also provided aggressive neonatal resuscitation to all live births. These perinatal cares were given with parental consent. In contrast, CS was not recommended at 23 weeks of gestation; however, we provided it following a parental request after offering an informed choice between vaginal and cesarean birth for obstetrical indications. Moreover, antenatal corticosteroid treatment for mothers with preterm labor prior to 24 weeks was not routinely given at our institution. All neonates born at 23 weeks of gestation were fully resuscitated and cared by neonatologists [10,11]. We first compared clinical characteristics such as the incidence of ROM, Abruption, IUGR, NRFHRs, intrauterine infection, severe preeclampsia, parental refusal of CS for obstetrical indication, breech delivery, CS delivery, and puerperal infection between 23 weeks and 24–26 weeks. Cases of intrauterine infection followed by NRFHRs were categorized as intrauterine infection. The incidence of poor outcome including cerebral palsy and neonatal death was also compared between 23 weeks and 24–26 weeks. Patients were then divided into 3 groups comprising NRFHRs, intrauterine infection, and ‘other’ (in labor) according to the presence of fetal
Admission FHR monitoring Reassuring
NRFHRs
R/O IUI Absent
In labor
Present
Labor induction
CS Delivery
Breech (Intrapartum) FHR monitoring NRFHRs Fig. 1. Perinatal management for 24–26 weeks. IUI: intrauterine infection. NRFHR: non-reassuring fetal heart rate pattern.
S. Furukawa et al. / Early Human Development 90 (2014) 113–118
indications to terminate pregnancy. The incidence of indications based on poor outcome was compared between 23 weeks and 24–26 weeks. Finally, in order to elucidate the effect of CS for obstetrical indication on neonatal outcome, we categorized each case as either a cesarean or vaginal birth when obstetrical indications were present. At this time, cases of intrauterine infection followed by NRFHR or intrauterine infection with breech presentation were also candidates for CS. Univariate analysis was first performed to determine the effect of CS for obstetrical indication on poor outcome at the respective weeks of gestation. We considered the effect of co-existing deteriorating factors on neonatal outcome except for obstetrical indication, and multiple logistic analysis was then performed using dichotomous variables. Data are expressed as number, incidence (%), mean ± SD, or range. Comparisons between groups were made using the Student's t-test or χ2 tests. Probability values b0.05 were considered significant.
3. Results At 23 weeks, the CS rate was 47% (16/34) and was significantly lower than 70% (64/91) at 24–26 weeks (p = 0.01). There was no significant difference between groups concerning maternal age, ROM, Abruption, IUGR, breech delivery, puerperal infection, or NRFHRs (Table 1). There were no cases of severe eclampsia at 23 weeks. The incidences of intrauterine infection (p = 0.02) and parental refusal of CS for obstetrical indication (p b 0.01) were significantly higher at 23 weeks than those at 24–26 weeks. The incidence of poor outcome was significantly higher at 23 weeks (65%) than at 24–26 weeks (34%, p b 0.01, Table 2). Sixteen cases of NRFHR were found at 23 weeks. Two cases were detected on admission following FHR monitoring. Among the 16 cases, 4 were CP and 7 were ND. On the other hand, 43 cases of NRFHRs were found at 24–26 weeks. Ten cases were detected on admission following FHR monitoring. Among the 43 cases, 12 were CP and 3 were ND. The incidence of a poor outcome was significantly higher at 23 weeks (p = 0.02) (Fig. 2A). Ten cases of intrauterine infection were found at 23 weeks, among which 4 were CP and 2 were ND. On the other hand, 11 cases of intrauterine infections were found at 24–26 weeks and included 4 cases of CP and one case of ND. There was no significant difference concerning the incidence of a poor outcome between groups (p = 0.50, Fig. 2B). Eight cases of the ‘other’ group were found in the 23-week group, among which 5 were CP. On the other hand, 26 cases were categorized as ‘other’ for the 24–26week group, among which 5 were CP and 3 were ND. There was no significant difference concerning the incidence of a poor outcome between groups (p = 0.11). Table 1 Maternal characteristics associated with infants born at 23 and 24–26 weeks of gestation. Results are expressed as number, mean ± SD, or incidence (%). Comparisons were made using the Student's t-test or χ2 tests. ROM: rupture of membrane; Abruption: placental abruption; IUGR: intrauterine growth restriction; NRFHR: non-reassuring fetal heart rate pattern; CS: cesarean section. Gestational age at birth Number
23 34
24–26 91
p
Maternal age (yr) ROM (%) Abruption (%) IUGR (%) NRFHR (%) Intrauterine infection (%) Severe preeclampsia (%) Refusal of CS for obstetrical indication (%) Breech delivery (%) CS delivery (%) Puerperal infection
28.7 ± 5.5 19 (56) 9 (26) 2 (6) 16 (47) 10 (29) 0 (0) 10 (29) 8 (24) 16 (47) 4 (12)
30.1 ± 5.3 37 (41) 20 (22) 15 (16) 43 (47) 11 (12) 11 (12) 4 (4) 11 (12) 64 (70) 6 (7)
0.20 0.13 0.60 0.35 0.98 0.02 0.08 b0.01 0.10 0.01 0.27
ROM: rupture of membrane, Abruption: placental abruption, IUGR: intrauterine growth restriction, NRFHR: non-reassuring fetal heart rate pattern, CS: cesarean section.
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Table 2 Demographic data of infants at 23 and 24–26 weeks of gestation. Gestational age at birth Number
23 34
24–26 91
p
Sex; girl (%) Weight (g, mean ± SD) IVH ≥ Grade III (%) Poor outcome (%) Cerebral palsy Neonatal death
12 (35) 577 ± 82 12 (35) 22 (65) 13 9
49 (54) 700 ± 123 8 (9) 31 (34) 23 8
0.06 b0.01 b0.01 b0.01
IVH: intraventricular hemorrhage.
We categorized each case as either a cesarean or vaginal birth when obstetrical indications were present at 23 weeks (Fig. 3). Five cases without obstetrical indications for CS resulted in a vaginal birth. Among women who presented obstetrical indications for CS with or without parental refusal at 23 weeks (n = 29), 16 cases involved a cesarean birth (n = 13) and the others resulted in a vaginal birth (n = 16). Then, cases that involved those who underwent vaginal birth with obstetrical indications (n=16) were defined as poor management. While, cases that involved a cesarean or vaginal birth without obstetrical indications (n = 18) were defined as normal management. The incidence of a poor outcome was compared between these two management groups. Eight infants in the normal management group had a poor outcome, while 14 infants in the poor management group exhibited a poor outcome. When the delivery was not managed according to the obstetrical indication for CS (poor management) at 23 weeks, there was an 8-fold higher risk of a poor outcome (odds ratio: 8.2; 95% confidence interval: 1.3–51.4; p = 0.03). In contrast, a vaginal birth in cases of obstetrical indication for CS at 24–26 weeks did not increase the risk of a poor outcome (odds ratio: 0.8; 95% confidence interval: 0.2–3.5; p = 0.75). As intrauterine infections were frequently seen at 23 weeks, we performed multiple logistic analysis after adjusting for intrauterine infection and vaginal birth on neonatal outcome. Vaginal birth in cases of obstetrical indication for CS more significantly affected poor outcome at 23 weeks (odds ratio: 13.0; 95% confidence interval: 1.3–129.6; p =0.03). Intrauterine infection did not affect poor neonatal outcome at 23 weeks (odds ratio: 0.3; 95% confidence interval: 0.03–4.3; p = 0.33). 4. Discussion We showed that poor neonatal outcome at 23 weeks of gestation was closely related to vaginal birth in cases of obstetrical indication. When obstetrical indication for CS existed at 23 weeks, a vaginal birth was associated with a 13-fold increased risk of a poor outcome compared to cases involving a CS birth. The incidence of a poor neonatal outcome was significantly higher in the NRFHR group at 23 weeks than at 24–26 weeks, although the incidence of NRFHRs was similar. It is worth noting that parental refusal of CS for fetal indication was higher at 23 weeks (p b 0.01). Intrauterine infection was frequently observed at 23 weeks, which is consistent with our previous reports that inflammation is an important prognostic factor in extremely premature infants ≤25 weeks of gestation [12,13]. In this study, there was no difference in the incidence of intrauterine infection-related poor outcome between 23 weeks and 24–26 weeks, except for CS indication. In addition, we showed that intrauterine infection was not an independent factor that deteriorated neonatal outcome at 23 weeks in spite of the high incidence of intrauterine infection. Some recent reports indicate that intrauterine infection is not an independent risk factor for poor prognosis in premature infants [14–16]. These conflicting reports may suggest that intrauterine infection does not have a direct causal relationship with poor outcome in extremely premature infants. The effect of intrauterine infection on neonatal prognosis may be augmented by the presence of other risk factors such as gestational age, IUGR or birth asphyxia, as we previously
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A) NRFHR
B) Intrauterine Infection
p=0.02
p=0.50
100%
100%
90%
90%
80%
80%
70%
70%
60%
60%
50%
50%
40%
40%
30%
30%
20%
20%
10%
10%
0%
Poor outcome
0% 23
24-26
23
24-26
Gestational age at birth (weeks) Fig. 2. A. Comparison of NRFHR-related poor outcome between 23 weeks and 24–26 weeks. Poor outcome included cerebral palsy and neonatal death. NRFHR: non-reassuring fetal heart rate pattern. B. Comparison of intrauterine infection-related poor outcome between 23 weeks and 24–26 weeks. Poor neonatal outcome included cerebral palsy and neonatal death.
reported [13]. There is no difference in the management strategy for intrauterine infection from 23 to 26 weeks in this study. Our uniform management strategy in cases of intrauterine infection may also involve decreasing the association with worsening prognosis. On the other hand, the incidence of poor neonatal outcome was significantly higher in the NRFHR group at 23 weeks than at 24–26 weeks. There was a difference in the management strategy for NRFHR between 23 weeks and 24–26 weeks in the present study. However, all neonates born at 23–26 weeks of gestation were equally resuscitated [10,11]. Thus, obstetrical management greatly impacted neonatal outcome when involving NRFHR at 23 weeks. Cesarean delivery during the peri-viable period may reduce hemodynamic stress during labor. We have reported that intrapartum severe variable deceleration is associated with subsequent intestinal perforation in extremely premature infants [10]. We speculated that preventing prolonged periods of hazardous decelerations could reduce peripheral tissue hypoxia and prevent subsequent intestinal perforation. We have also shown that in poor-outcome infants born at 22–24 weeks of gestation, the catecholamine and volume load increased significantly to maintain adequate blood pressure and urination [11]. Thus, vaginal delivery during the peri-viable period induced hazardous NRFHRs and potentially affected cardiovascular stability. However, the beneficial effect of cesarean delivery during the peri-viable period is controversial [17]. One of the reasons for the inconsistent results is that the study population includes unadjusted co-existing factors such as intrauterine infection, IUGR, parental refusal, and the attitude of the physician. According to our results, vaginal birth in cases of obstetrical indication for CS did not affect neonatal outcome at 24–26 weeks, but produced an effect at 23 weeks. In Sweden, two different regional strategies for perinatal management of extreme prematurity co-existed, and indicated that CS for obstetrical indication was associated with improved neonatal outcome from 22 to 25 weeks without increased morbidity [18]. Due to the difficulty of conducting a controlled study, a comparison of different strategies within a homogenous group or comparison of different regional strategies is the only feasible method to prove the effectiveness of CS for obstetrical indication. Both studies support CS for obstetrical indication in extreme prematurity, particular at 23 weeks of gestation. Maternal complication associated with CS during the peri-viable period is an important matter for future pregnancies. A report from
the Cochrane Database indicated there was a significant advantage for women to undergo a preterm vaginal delivery compared to a preterm CS delivery with respect to maternal infection [17]. In our study, four cases of puerperal infection were found at 23 weeks, and three of the four cases involved CS. Likewise, six cases of puerperal infection were found at 24–26 weeks, and all involved CS. Obviously, the incidence of puerperal infection was high for cesarean section. Puerperal infection is one of the causes of infertility. Another concern for preterm CS is the potential risk of uterine rupture in the next pregnancy. We previously reported subsequent pregnancy outcomes (n = 103) in cases involving a vertical uterine incision for premature birth [19]. In this series, 33% (34/103) of patients were pregnant and the incidence of uterine rupture was 0% (0/32). Due to the small number of cases in that study, it is difficult to determine whether there is low risk of uterine rupture in subsequent pregnancy. Currently, there is no advantage for maternal health in preterm CS delivery. It is important to note that this study has some limitations. First, the current study involved only one tertiary hospital. Second, we did not consider the effect of steroid administration. Antenatal corticosteroid treatment before 24 weeks of gestation has been shown to improve neonatal outcome [20,21]. We did not routinely use antenatal corticosteroid treatment before 24 weeks; however, all neonates born at 22– 24 weeks received surfactant replacement therapy and hydrocortisone for circulatory stabilization [10,11]. The outcomes of neonates should be documented to verify the effect of antenatal corticosteroid treatment for extreme prematurity in future pregnancies. Third, we did not include the effect of parental refusal as a co-existing deteriorating factor on neonatal outcome. We focused on cases involving those who underwent vaginal birth with obstetrical indications for CS with or without parental refusal. In conclusion, we demonstrated that vaginal birth in cases of obstetrical indication for CS at 23 weeks resulted in a 13-fold higher risk of a poor outcome. Our results imply that neonates at 23 weeks would receive some benefit from a CS for obstetrical indication, compared with a vaginal birth.
Conflict of interest There is no relationship that might lead to a conflict of interest.
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117
Admission FHR monitoring Reassuring
NRFHR : 2
R/O IUI
Without IUI : 22
Vaginal birth
1 (Intrapartum) FHR monitoring
6
3
In labor Breech : 6 NRFHR : 7 NRFHR+Breech : 7 Reassuring: 2
POOR MANAGEMENT GROUP Reassuring R/O IUI
With IUI : 10 Vaginal birth
Labor induction: 9
1
In labor: 1
(Intrapartum) FHR monitoring
2
3
Breech : 1 NRFHR : 3 NRFHR+Breech : 3 Reassuring: 3
Fig. 3. Consequence of delivery in relation to obstetrical indication for cesarean section at 23 weeks. Upper part: cases with NRFHRs on admission and cases without IUI. Lower part: cases with IUI. IUI: intrauterine infection.
Acknowledgment This work was supported in part by a grant from the JAOG Ogyaa Donation Foundation and a grant (#79-258) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Parts of this study were presented as an oral presentation at The 47th Symposium of the Japan Society of Perinatal and Neonatal Medicine in Sapporo, Japan, 2011.
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