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Maternal risk factors and obstetric complications in late preterm prematurity

European Journal of Obstetrics & Gynecology and Reproductive Biology 179 (2014) 105–109

Abstract

Objective

Late preterm prematurity has been related to poorer neonatal outcomes. However, research has focused on the neonatal outcomes of late preterm infants, maternal characteristics of these births have been less evaluated. The aim of the study was to compare maternal risk factors and obstetric complications in late preterm births (LPTB) and term births. These factors were also assessed comparing spontaneous LPTB with medically-indicated LPTB.

Study design

We conducted a retrospective cohort study with two groups. All singleton LPTB occurred at our University Hospital between January 1, 2009 and December 31, 2010 were included in the first cohort (n = 171). A comparison cohort of term births was configured in a ratio 2:1 (n = 342). Well-dated pregnancies without congenital malformations, congenital infections or chromosome abnormalities were eligible. LPTB were classified into two groups, spontaneous LPTB and medically-indicated LPTB following delivery indications. Statistical analysis of categorical variables was performed using either χ2 or Fisher’s exact. Continuous variables were compared using the Student’s t-test.

Results

Women with LPTB had more medical conditions than women with term births (29% vs 15.7%; P = 0.002). Prior preterm births (9.7% vs 2%; P < 0.001), prior adverse obstetric outcomes (6.9% vs 2.3%; P < 0.001), and obstetric complications were also more frequent in LPTB than in term births. However, no differences were found in maternal medical conditions when spontaneous LPTB and medically-indicated LPTB were compared. Women with medically-indicated LPTB were older (33.69 vs 31.07; P = 0.003) and mainly nulliparous (75.8% vs 49.4%; P = 0.002). Obstetric complications were more frequent in medically-indicated LPTB than in spontaneous LPTB.

Conclusions

Maternal risk factors and obstetric complications are significantly higher in LPTB than in term births. These factors should be considered to identify women at risk for either spontaneous or medically-indicated LPTB.

Keywords: Late preterm birth, Maternal risk factors, Obstetric complications, Prematurity.

Introduction

Prematurity rates have increased in recent years mainly due to an increase in late preterm births (LPTB) [1], [2], and [3], defined as births occurring between 34 0/7 and 36 6/7 weeks. This group currently represents nearly 75% of preterm births (PTB). Several factors have been suggested to contribute to the increase in prematurity rates. One proposed explanation is that changes in maternal factors, such as the rise of maternal age at pregnancy and assisted reproduction techniques, may have increased the number of high-risk pregnancies, which are at higher risk of prematurity [2] . Another possible explanation is that pregnancies at risk for an adverse perinatal outcome are often delivered before term. This could be due to a more comprehensive understanding of fetal adaptation mechanisms to threatening situations [4] and [5]. The enhancements in obstetric surveillance and neonatal care have also been cited as partially responsible for the increase in prematurity rates [2] .

Late preterm prematurity has been related to poorer neonatal outcome [6], [7], [8], and [9]. Teune et al. [9] performed a systematic review, comparing neonatal morbidity in LPTB to term births. The authors reported higher rates of respiratory distress syndrome, intraventricular hemorrhage, necrotizing enterocolitis and neonatal death in late preterm infants. Long-term outcomes, such as mortality in the first year of life, neurological development and school performance, were also worse in LPTB. These results have increased concern among obstetric and pediatric communities [10] , and indications for delivery in LPTB have been investigated [11] and [12].

Previous studies suggest that only a few LPTB are avoidable, since these preterm births often occur following a maternal or obstetric complication [13] . However, although extensive research has been conducted on LPTB, few studies have evaluated the maternal and obstetric factors specifically associated with this situation. Differences in maternal and obstetric characteristics between spontaneous and indicated LPTB also remain unknown. Better knowledge of the maternal risk factors involved in LPTB may allow to identify patients at risk for LPTB. Better knowledge of the obstetric complications associated with LPTB may help to determine which situations would benefit from conservative management, without increasing maternal and perinatal risks by continuing the pregnancy. We therefore conducted a retrospective cohort study to evaluate maternal risk factors and obstetric complications in singleton pregnancies delivered between 34 0/7 and 36 6/7 weeks at our institution. We assessed these factors by comparing LPTB with term births, and spontaneous LPTB with medically-indicated LPTB.

Material and methods

We performed a retrospective cohort study of all singleton LPTB delivered at Hospital de la Santa Creu i Sant Pau in Barcelona, a tertiary university hospital, between January 1, 2009 and December 31, 2010. A control cohort of term births (37 0/7–41 6/7 weeks) was randomly configured in a 2:1 ratio. Approval for the study was obtained from the ethics committee of the Institutional Review Board at Hospital de la Santa Creu i Sant Pau, Barcelona.

Eligible cases were identified from the delivery room logbook, and maternal and pregnancy data were reviewed. Well-dated and well-controlled singleton pregnancies with a live fetus at hospital admission were accepted for statistical analysis. Only pregnancies with first-trimester ultrasound assessment of gestational age were considered well-dated. Exclusion criteria for both the study and control groups were major anatomic malformations, chromosome abnormalities and congenital infections.

Data were collected through retrospective chart review. We recorded information on maternal age, parity, prior uterine surgery, artificial reproductive technique (ART), history of PTB, and history of adverse obstetric outcome (defined as 3 or more miscarriages, second trimester fetal loss, prior fetal major malformation or prior chromosome abnormality). Presence of maternal medical disorders was reviewed. We considered for analysis hypertensive, endocrinological (thyroid disorders and diabetes), autoimmune and prothrombotic disorders. Congenital heart diseases and infectious conditions were also noted. Other maternal medical disorders (e.g. neurological, psychiatric, rheumatic or respiratory conditions) were considered as “others” for the analysis. This category included medical conditions that are less likely to be linked to pregnancy-related complications. We created a composite variable to measure maternal medical disorders. This variable, composite maternal morbidity, was defined as the presence of one or more medical disorders.

Pregnancy-related complications analyzed were hypertensive disorders of pregnancy (gestational hypertension and preeclampsia), intrauterine growth restriction (IUGR), intrahepatic cholestasis of pregnancy, gestational diabetes, and bleeding in the second half of pregnancy (abruptio placentae, placenta previa). Other pregnancy-related complications (e.g. urinary tract infections, ovarian hyperstimulation syndrome, alterations in the quantity of amniotic fluid, maternal anemia) were considered as “others” for the analysis. We also recorded maternal antenatal care requirements (admission to the High Risk Obstetric Unit, antenatal corticosteroid and tocolytic treatment). Finally, indication for delivery and mode of delivery were noted. The study investigators jointly resolved all uncertainties and discrepancies in the medical charts.

For comparative purposes, LPTB were classified into two groups, spontaneous LPTB and medically-indicated LPTB. We considered LPTB was spontaneous when preterm premature rupture of membranes (PPROM) or spontaneous preterm labor (SPTL) occurred between 34 0/7 and 36 6/7 weeks, as in these cases our current protocols recommend immediate delivery. Women admitted to hospital for SPTL or PPROM in the late preterm period were included in the spontaneous group even if they presented other obstetric complications. We considered LPTB as medically-indicated when delivery occurred following an obstetric or maternal complication. As established in our institutional protocols, when PPROM occurred before 34 0/7 weeks, conservative management was adopted after excluding chorioamnionitis criteria. If pregnancy reached 34 0/7 weeks, labor was induced and prematurity was classified as medically-indicated.

A specific database was created, and a spreadsheet format was used for statistical analysis. Statistical analysis was performed using SPPS (version 17.0, SPSS Inc., Chicago IL). Associations between categorical variables were evaluated using either χ2 or Fisher’s exact test where necessary. The Mann–Whitney U test was used for ordinal variables. Continuous variables were compared using the Student's t-test. Both the variables that were statistically significant in the univariate analysis, and the variables that were considered clinically relevant, were further investigated using multivariate logistic regression analysis. A P value < 0.05 was used to define statistical significance.

Results

During the two-year study period, there were 3545 singleton live births at our institution, 6.43% (n = 228) of which were singleton PTB. Out of the 228 singleton PTB, 74.9% (n = 171) were singleton LPTB. A control group of 342 term births was randomly configured. Of the 171 LPTB and 342 term births selected for the study, 84.8% (n = 145) and 87.4% (n = 299), respectively, met selection criteria and were eligible for analysis. Fig. 1 shows the study sample selection process. In the LPTB group, 19.3% (n = 28) infants were delivered at 34 (34 0/7–34 6/7) weeks, 25.6% (n = 40) at 35 (35 0/7–35 6/7) weeks, and 53.1% (n = 77) at 36 (36 0/7–36 6/7) weeks.

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Fig. 1 Diagram of included and excluded patients. This figure shows the study profile. Causes for patient exclusion are also detailed.

Maternal clinical characteristics of LPTB and term births are described in Table 1 . No differences were found with regard to maternal age, parity, ART or prior uterine surgery. History of PTB and prior adverse obstetric outcome were more frequent in LPTB than in full-term pregnancies (9.7% vs 2%; P < 0.001, and 6.9% vs 2.3%; P < 0.05, respectively). Composite maternal morbidity rate was also significantly higher in women with LPTB (29% vs 15.7%; P < 0.01). Endocrinological disorders were the most frequent medical disorders in both LPTB and term groups, followed by prothrombotic conditions.

Table 1 Maternal clinical characteristics of the late preterm and term groups.

Maternal characteristic Late preterm (n = 145) Term (n = 299) P value
Maternal age, (years) a 32.19 ± 5.33 31.84 ± 5.10 0.511
Nulliparity, n (%) 88 (60.7) 187 (62.5) 0.755
Prior uterine surgery, n (%) 16 (11.1) 24 (8) 0.295
History of preterm birth, n (%) 14 (9.7) 6 (2) <0.001 *
History of adverse obstetric outcome, n (%) 10 (6.9) 7 (2.3) 0.031 *
Artificial reproductive technique, n (%) 13 (9) 16 (5.4) 0.156
Composite maternal morbidity, n (%) 42 (29) 47 (15.7) 0.002 *
Hypertensive disorder, n (%) 4 (2.8) 1 (0.3)  
Endocrinological disease, n (%) 11 (7.6) 16 (5.4)  
Prothrombotic condition, n (%) 11 (7.6) 5 (1.7)  
Congenital heart disease, n (%) 2 (1.4) 1 (0.3)  
Infectious condition, n (%) 2 (1.4) 4 (1.3)  
Cervical conization, n (%) 1 (0.7) 2 (0.7)  
Other, n (%) 16 (11.1) 18 (6)  

* Denotes significant differences (P < 0.05).

a Data are given as mean ± SD.

The obstetric characteristics of LPTB and term groups are summarized in Table 2 . Rates of all reviewed pregnancy-related complications were significantly higher in the LPTB group. IUGR and intrahepatic cholestasis of pregnancy were the obstetric complications most frequently observed in LPTB (15.2% and 10.3%, respectively), whereas gestational diabetes was the most frequent complication in term births (4.3%). Women who delivered at late preterm period were more likely to require admission to the High Risk Obstetric Unit, antenatal corticosteroid and tocolytic treatments. As regards the mode of delivery, more than 40% of late preterm infants were delivered by caesarean section (42.8% vs 21.4%; P < 0.001).

Table 2 Obstetric characteristics of the late preterm and term groups.

Obstetric characteristic Late preterm (n = 145) Term (n = 299) P value
Maternal admission to the High Risk Obstetric Unit, n (%) 25 (17.4) 4 (1.3) <0.001 *
Corticosteroid therapy, n (%) 24 (16.7) 1 (0.3) <0.001 *
Tocolytic therapy, n (%) 19 (13.1) 0 (0) <0.001 *
 
Obstetric complications
Hypertensive disease, n (%) 11 (7.6) 6 (2) 0.007 *
Intrauterine growth restriction, n (%) 22 (15.2) 5 (1.7) <0.001 *
Intrahepatic cholestasis of pregnancy, n (%) 15 (10.3) 2 (0.7) <0.001 *
Gestational diabetes, n (%) 14 (9.7) 13 (4.3) 0.035 *
Bleeding in the second half of pregnancy, n (%) 7 (4.8) 4 (1.3) 0.045 *
Other, n (%) 10 (6.9) 26 (8.7) 0.582
 
Mode of delivery
Vaginal delivery, n (%) 83 (57.2) 235 (78.6) <0.001 *
Operative vaginal delivery, n (%) 18 (21.7) 77 (32.7) <0.001 *
Caesarean section, n (%) 62 (42.8) 64 (21.4) <0.001 *

* Denotes significant differences (P < 0.05)

Composite maternal morbidity, obstetric complications, history of PTB, prior adverse obstetric outcome and ART were included in the multivariate analysis. Only composite maternal morbidity (OR 1.86; 95% CI, 1.11–3.09), obstetric complications (OR 3.83; 95% CI, 2.44–6.04), and history of PTB (OR 5.08; 95% CI, 1.80–14.31), remained significantly associated with LPTB (data not showed in tables).

Of the 145 LPTB analyzed, 57% (n = 83) were spontaneous and 43% (n = 62) were medically-indicated. In the spontaneous group 13 neonates were born at 34 weeks, 27 at 35 weeks, and 43 at 36 weeks. In the medically-indicated group 15 neonates were delivered at 34 weeks, 13 at 35 weeks, and 34 at 36 weeks. Distribution by gestational age at delivery showed no differences between groups (P = 0.207). Medically-indicated LPTB were mainly due to an obstetric complication, and only two cases occurred exclusively as a result of a maternal situation (one elective delivery at 36 weeks in a woman with a high-risk prothrombotic condition, and one elective delivery at 36 weeks in a woman with severe gastroenteritis). Three pregnancies were complicated by PPROM before 34 0/7 weeks (one case at 26 weeks, and two cases at 33 weeks). Conservative management was adopted after excluding chorioamnionitis, and labour was induced at 34 weeks. These cases were categorized as medically-indicated, in accordance with the study protocol.

Differences in maternal and obstetric characteristics were assessed comparing spontaneous LPTB with medically-indicated LPTB ( Table 3 ). Women with medically-indicated LPTB were more likely to be older and nulliparous, but no differences were found between the two groups in the composite maternal morbidity rate (33.9% vs 25.3%; P = 0.273). As medically-indicated LPTB were defined as deliveries occurring following an obstetric or maternal complication, pregnancy-related complications were more frequent in this group. Table 4 illustrates these results. Maternal antenatal care was equally required in both groups. Conversely, caesarean rate was significantly higher in medically-indicated LPTB (74.2% vs 19.3%; P < 0.001). Composite maternal morbidity, obstetric complications, maternal age, nulliparity, history of PTB, ART were included in the multivariate analysis. The only variable that was significantly associated with medically-indicated LPTB was the presence of an obstetric complication (OR 46.48; 95% CI, 17.16–125.92) (data not showed in tables).

Table 3 Maternal clinical characteristics of the spontaneous and medically-indicated LPTB.

Maternal characteristics Spontaneous LPTB (n = 83) Medically- indicated LPTB (n = 62) P value
Maternal age, (years) a 31.07 ± 5.18 33.69 ± 5.19 0.003 *
Nulliparity, n (%) 41 (49.4) 47 (75.8) 0.002 *
Prior uterine surgery, n (%) 12 (14.5) 4 (6.5) 0.181
History of preterm birth, n (%) 9 (10.8) 5 (8.1) 0.777
History of adverse obstetric outcome, n (%) 5 (6) 5 (8.1) 0.582
Artificial reproductive technique, n (%) 7 (8.4) 6 (9.7) 1
Composite maternal morbidity, n (%) 21 (25.3) 21 (33.9) 0.273
Hypertensive disorder, n (%) 1 (1.2) 3 (4.8)  
Endocrinological disease, n (%) 6 (7.2) 4 (6.5)  
Prothrombotic condition, n (%) 4 (4.8) 7 (11.3)  
Congenital heart disease, n (%) 1 (1.2) 1 (1.6)  
Infectious condition, n (%) 2 (2.4) 0 (0)  
Cervical conization, n (%) 0 (0) 1 (1.6)  
Other, n (%) 10 (12) 6 (9.7)  

* Denotes significant differences (P < 0.05).

a Data are given as mean ± SD.

Table 4 Obstetric characteristics of the spontaneous and indicated LPTB.

Obstetric characteristic Spontaneous LPTB (n = 83) Medically-indicated LPTB (n = 62) P value
Maternal admission at High Risk Obstetric Unit, n (%) 12 (14.6) 13 (21) 0.377
Corticosteroid therapy, n (%) 13 (15.9) 11 (17.7) 0.823
Tocolytic therapy, n (%) 13 (15.7) 6 (9.7) 0.330
 
Obstetric complications
Hypertensive disease, n (%) 0 (0) 11 (17.7) <0.001 *
Intrauterine growth restriction, n (%) 2 (2.4) 20 (32.3) <0.001 *
Intrahepatic cholestasis of pregnancy, n (%) 1 (1.2) 14 (22.6) <0.001 *
Gestational diabetes, n (%) 6 (7.2) 8 (12.9) 0.270
Bleeding in the second half of pregnancy, n (%) 2 (2.4) 5 (8.1) 0.138
Other, n (%) 2 (2.4) 8 (12.9) 0.019 *
Mode of delivery     <0.001 *
Vaginal delivery, n (%) 67 (80.7) 16 (25.8)  
Caesarean section, n (%) 16 (19.3) 46 (74.2)  

* Denotes significant differences (P < 0.05).

Comment

Our study showed that women with LPTB had more medical disorders, mainly endocrinological and prothrombotic conditions. However, no differences were observed when spontaneous and medically-indicated LPTB were compared. We have also identified other maternal risk factors highly associated with LPTB. According to our data, the rate of prior PTB was up to 5-fold higher in LPTB, corroborating findings from previous studies assessing recurrence of PTB [14] . However, no differences were noted in prior PTB rate when we compared spontaneous and medically-indicated LPTB. The rate of ART was similar in LPTB and term births. One possible explanation for this finding is that we only included singleton pregnancies, and risk of prematurity in pregnancies achieved through ART is mainly associated with multiple pregnancies. According to our results, prior PTB, history of adverse obstetric outcome, and the presence of maternal medical conditions were equally associated with spontaneous and medically-indicated LPTB. This suggests these factors are not suitable to distinguish women at risk for spontaneous LPTB from women at risk for medically-indicated LPTB. As expected, the risk of developing obstetric complications during pregnancy was increased in LPTB. This increase was also observed in medically-indicated LPTB as compared with spontaneous LPTB. IUGR and cholestasis were the most frequent obstetric complications in LPTB, whereas these complications were rare in term births. Our current protocols recommend earlier delivery in many cases of IUGR and cholestasis. This may explain the differences in obstetric complications between LPTB and term births.

Multiple maternal factors have been related to PTB [15] . However, these factors have not been so well studied in the late preterm period. We observed that prematurity risk factors also have a significant role in LPTB. Shapiro-Mendoza et al. [16] showed that maternal medical conditions are associated with a higher risk for neonatal morbidity. Our study adds to their conclusions that maternal medical disorders can be helpful in identifying women at risk for LPTB. Pregnancy-related complications have also been associated with both spontaneous and medically-indicated LPTB [6] and [12]. Our findings are consistent with these results. Hypertensive disorders of pregnancy have been reported as the most frequent obstetric complication in LPTB [12] , whereas in our study the most frequent complication was IUGR. However, hypertensive disorders and IUGR were together responsible for 42% of medically-indicated LPTB. This supports the finding that placental disease and indicated prematurity are intimately related.

Indications for delivery in LPTB have been previously investigated. In our study more than 40% of LPTB were medically-indicated, which is a higher rate than those published by other authors [12] and [17] (31.8% and 32.3%, respectively). This might be explained by the fact that our center is a tertiary referral hospital for high-risk pregnancies. As in our study, Gyamfi-Bannerman et al. [12] classified LPTB as spontaneous or non-spontaneous according to indication for delivery. They further categorized non-spontaneous LPTB as evidence-based or non-evidence based births, and concluded that 56.3% of indicated deliveries were non-evidence based. Our study did not aim to evaluate indications for delivery in LPTB. We thus reported maternal and obstetric complications without distinguishing between evidence and non-evidence based deliveries. It is likely that some medically-indicated LPTB included in our study were non-evidence based, and this might also explain the high rate of indicated deliveries in the LPTB group.

To our knowledge, this is the first study comparing maternal clinical characteristics of spontaneous and medically-indicated LPTB. We found that women with medically-indicated LPTB were significantly older and more frequently nulliparous. Maternal age and nulliparity have been recognized as risk factors for several obstetric complications [18] and [19]. In Spain, maternal age at pregnancy has increased over the past years (from 28.2 years in 1980 to 31.3 years in 2011), and this increase has been more pronounced than in other European countries. However, maternal age and nulliparity are conflicting risk factors. These factors were included in the multivariate analysis, and only obstetric complications remained significantly associated with medically-indicated LPTB. Thus, older and nulliparous pregnant women should be considered at risk both for an obstetric complication and a medically-indicated LPTB. We also evaluated antenatal care requirements of LPTB. Obstetric complications were more frequent in LPTB, and maternal antenatal care was subsequently more necessary in this group. On the contrary, antenatal care requirements were similar in spontaneous and medically-indicated LPTB, despite higher rates of obstetric complications in the indicated group. Our results suggest that spontaneous and medically-indicated LPTB should not be considered together when evaluating LPTB.

The chart review of every patient included in our study allowed a more accurate data assessment than abstraction from large databases. We only accepted deliveries with first-trimester ultrasound assessment of gestational age, which is more precise than dating from the last menstrual period. Additionally, only pregnancies delivered in the late preterm period were included, whereas other studies evaluating late preterm prematurity also included 33-week births. We believe 34 weeks is an important time reference to evaluate causes and consequences of prematurity.

Our study has some limitations. Firstly, pregnancy-related complications were assessed without considering the severity of the condition, information of interest when assessing the obstetric characteristics of LPTB. Secondly, our study was not adequately powered to establish relationships between the presence of maternal medical disorders and the occurrence of obstetric complications. Another debatable aspect is the sample size of the LPTB group for the comparison of spontaneous and medically-indicated LPTB. We cannot conclude that these results would persist with a larger sample, although we believe our findings have a clinical significance.

The increase in LPTB is due to a rise in medically-indicated LPT [20] and [21], a rise that has led to a decline in stillbirths and neonatal deaths [22] . At the same time, however, research suggests that neonatal morbidity is higher in late preterm infants than in term infants [10], [23], and [24], and these results have been confirmed in low-risk spontaneous LPTB [25] . This excess of neonatal morbidity and the increase in medically-indicated LPTB rates are therefore controversial [26] and [27], and studies assessing whether LPTB are avoidable have reached conflicting conclusions [13], [17], and [26]. This suggests that risks and benefits of medically-indicated preterm deliveries must be individually assessed at every gestational age, including the late preterm period.

Our results suggest that clinical and obstetric risk factors may help identify women at risk for LPTB. Our study also provides information on the maternal and obstetric differences between spontaneous and medically-indicated LTPB. Although more data are needed to address these differences, we believe it is important to consider spontaneous and medically-indicated LPTB as two different conditions, both clinically and in research. Clinical practice guidelines should insist on maternal clinical characteristics for a thorough identification of patients at risk for LPTB. Better assessment of both maternal and fetal risks of obstetric complications at late preterm period is needed.

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Footnotes

a Department of Obstetrics and Gynecology, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain

b Department of Pediatrics, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain

lowast Corresponding author at: Hospital de la Santa Creu i Sant Pau, Department of Obstetrics and Gynecology, C/Sant Quintí 89, Barcelona 8025, Spain. Tel.: +34 935537041.