Introduction
Caesarean section (CS) rate is rising dramatically around the world [
1]. WHO Global Survey of Maternal and Perinatal Health (WHOGS; 2004–08) and WHO Multi-Country Survey of Maternal and Newborn Health (WHOMCS; 2010–11) have shown that the CS rate increased overall between the two surveys (from 26·4% in the WHOGS to 31·2% in the WHOMCS) in all countries except Japan. The rate is highest in China between the two surveys and has increased from 46.2 to 47.6% [
2]. Elective CS (ECS) scheduled before the labor is a major contributor to this uprising trend [
3]. The rate of CS on maternal request (non-indicated CS), a subgroup of ECS, is high and growing. It has accounted for 4–18% of CS births in USA and for 36% in south-east China and thus becomes an emerging global public health concern [
4,
5].
Childhood psychopathology related to mode of delivery has drawn wide attention recently. Emotional and behavioral problems are areas that require more concern because they are potentially modifiable and are related with later-life social development [
6]. Researchers have studied the effect of delivery mode on children’s development in these areas, but the conclusions are controversial. Some studies have observed developmental delay in personal social and gross motor domains [
7] and more emotional disturbances among children born from maternally-requested ECS [
8]. While others reported no association [
9] or even an association between maternally-requested ECS and a lower risk of childhood psychopathological problems [
3].
Simultaneously, mean gestational age has decreased globally [
10]. This trend is primarily owing to the rise in ECS [
11]. The absolute increase of 8.9% of early term infants (defined as 37–38 gestational weeks) during the past decade in USA is largely due to an increase in CS on request [
12]. A regional audit has shown that 44% of ECS was carried out before 39 weeks, maternal request being one of the top three reasons for ECS [
13]. Not just preterm birth will cause adverse consequences [
14,
15], early term birth, which was ever considered as term birth, is also recognized to have potentially detrimental health effect, such as increased mortality and hospital stay, greater complications in subsequent pregnancies, short-term respiratory morbidities and newborn intensive care admissionsin in elective early term births [
16‐
22]. Researchers also found a dose-dependent relationship of special education needs (SEN) with gestation. Communication impairments and lower general cognitive ability were more common in infants born early term and accounts for more cases of SEN [
14,
15].
Given the potential risks in CS on maternal request, educational and policy initiatives have been led to eliminate the non-indicated CS prior to 39 gestational weeks by American College of Obstetricians and Gynecologists and National Institute of Clinical Excellence [
23,
24]. Nevertheless, whether the recommendation can be universally applied is questionable as it is much based on physiological evidence or expert opinion [
25]. Neither group has acknowledged the children’s potential psychological risk. Meanwhile, the gestational age of fetal maturity may vary by race [
26], and there were notable racial disparities in race in serious neonatal morbidities in preterm infants [
27]. Previous researches on offspring’s emotional and behavioral development have simply concerned delivery mode and mostly by retrospective design [
3,
7,
8], or solely looked into the gestational age and highly inclined to preterm births [
28,
29]. The population-based prospective studies on the combinative effects of delivery mode and gestational length on psychological outcomes are scarce. In the present study, based on a Chinese birth cohort, we recruited women with singleton live births, investigated emotional and behavioral development in pre-school children born with non-indicated ECS at different gestational ages.
Discussion
In this prospective birth cohort study in China, the overall CS rate had reached 65.4%, and the rate of ECS on maternal request was 20.9%. The prevalence of ECS on maternal request prior to 39 weeks, at 39–40 weeks and beyond 41 weeks was 16.6, 23.7 and 15.9%, respectively. ECS on maternal request was the independent predictor of emotional problems and total difficult problems in children born prior to 39 gestational weeks at preschool age.
Although WHO has stated that no robust evidence existed for ideal CS rate, the rate observed in our study was very high. It was higher than that reported by WHO surveys [
2], and that observed in Shanghai (38.8%, 2007) and Wenzhou (50.3%, 2008) in China [
40,
41]. The rate of non-indicated ECS was lower than that in Shanghai (24.7%, 2007) while higher than that in Wenzhou (18.25%, 2008) [
40,
41].
It is reported that at population level, CS rates over 10% are not related with improvements in mothers and newborns [
42]. Previous studies failed to find significant associations between delivery mode and infant and childhood psychopathology [
43]. Even the least prevalence of emotional or behavioral problems in children born by ECS was reported [
3]. In our study, we observed a higher possibility of total difficult problems in children born by ECS on maternal request. When gestational age was concerned, the associations were centrally distributed in the group prior to 39 weeks. Most notably, higher prevalence of emotional problems in children born early term by ECS on maternal request was observed at the first time in our study. Interestingly, when emotional problems were controlled in regression model, the RR (95%CI) of total difficult problems for ECS on request prior to 39 weeks had changed to be 1.519(0.738–3.128). It implicated that the high possibility of total difficult problems in children with non-indicated ECS prior to 39 weeks was confounded by emotional problems. In other words, emotional problems might be the most important component in the overall emotional and behavioral abnormities in children born with ECS on maternal request prior to 39 gestational weeks. The increasing trend of preterm and early term deliveries is a growing and major public health concern [
15,
44]. Previous studies indicated higher prevalence for inattention-hyperactivity, emotional problems and peer problems in preterm children [
28,
29,
45,
46]. As far as conduct problems, results were much mixed and only a few studies found increased risk among very preterm children or children with very low birth weight [
29,
47].
The mechanisms underlying the association of lower gestational age and higher emotional and behavior problems in children born with ECS on maternal request are complex and unclear. One possible mechanism might be the “iatrogenic prematurity” [
12] that the pregnancy could be cut short when fetal brain development in the uterine is still going on [
48]. Perinatal intervention like CS could interrupt the development of prefrontal cortex and hippocampal neurons in the experimental animals [
49]. Hormonal secretion might be invoked to explain the association between ECS and children’s emotional and behavioral problems. The absence of labor will eliminate the release of stress hormones, such as glucocorticoid [
50]. This process might have re-programming potentials on hypothalamic-pituitary-adrenal (HPA) axis function and behavior and result to long-term effects on children’s neuropsychological development [
51,
52]. In this study, ECS with medical indications had shown a certain degree of protective effect on peer problems in children prior to 39 gestational weeks. Operative childbirth due to certain medical conditions was necessary intervention and could improve maternal and infant health outcomes. Its implication in protecting maternal and child health went beyond the process of labor, and the underlying beneficial neurodevelopmental effect on the children was quite different from non-indicated ECS.
The “39 week” rule for ECS on maternal request is mostly based on evidence of maternal and infant physiological effects in western populations. A potential psychological implication prior to 39 weeks in the present study has thus been added to the roster of impacts of ECS on maternal request. At various fetal maturity status, our conclusions have directed independent effect of ECS on request on children’s psychological outcomes and provided evidence-based data on maternal health providers’ and user’s decision-making of ECS and the optimal timing to perform it. The reasons for the very high overall CS rate and rate of ECS on maternal request are complex in China. Social/cultural factors, such as women’s fear of pain, selection of an auspicious birth day, bandwagon effect among maternal health users, as well as physician’s defensive medical behavior may play important major in the dramatic increase [
53,
54]. Due to the limited development in labor analgesia and deep-rooted cultural contexts in China, it might be difficult to reverse the situation in a short period. As a concession, the findings have important implications for clinical practice in China, where there is no definite guideline on optimal timing of the non-indicated CS. The health education is not only limited among the providers. It is more critical to communicate to pregnant women and their families on the negative consequences of early ECS, because most women believed that full term was reaching 37 gestational weeks and it was safe to deliver at that time when there were no other complications [
55]. Emotional and behavioral development should be closely monitored in children born with non-indicated ECS prior to 39 weeks in child health care service. Although the problems of early term are subtler than those of preterm babies, they are more numerous and thus possibly to be a greater burden for health services, and would benefit from more careful concern and assessment.
This study was a birth cohort design. The loss rate in the cohort was relatively low. It was around 4.2% from the 1st trimester of pregnancy to childbirth, and about 18.5% from delivery till 3–5 years after delivery. General characteristics of mother-infant pairs and children’s emotional and behavioral outcomes were collected prospectively so that recall bias was less likely to occur. This design also allowed for the inclusion of a large number of potential confounders. In particular, prenatal factors that might cause early elective childbirth and relate with offspring’s psychological development, such as prenatal stress and pregnant complications were fully considered and controlled. Differences in rate of prenatal anxiety were reported among different studies due to various population and instruments. The prevalence of pregnancy-related anxiety was 24.9 and 13.9% respectively in the 1st and 3rd trimester of pregnancy in our study. Other Chinese researchers reported maternal anxiety rate by using general anxiety scales. For example, with self-rating anxiety scale (SAS), 20.6% women had reported antenatal anxiety in late pregnancy [
56]. Yu Y et al. revealed that 22.6 and 21.0% women had maternal anxiety respectively in 1st and 3rd trimester of pregnancy [
57]. Pregnancy-related anxiety questionnaire developed by our team had been adopted by other researchers. 15.2 and 21.7% women were found to have maternal anxiety respectively in Shanghai [
58] and Zhejiang [
59], China.
Meanwhile, some weakness in the study must be acknowledged. Firstly, as to the participants, most of them were from urban areas. Maternal health service usage, breastfeeding situation and parenting style could be quite different between urban and rural families. Therefore, it should be prudent to explain our findings in rural areas. The overall prevalence of emotional and behavioral problems in pre-school children was reported to be 34.1 and 11.9% in rural areas respectively in Shandong and Hunan province, China [
60,
61], being higher than the rate observed in our urban sample (7.6%). Secondly, in terms of the outcomes, although SDQ was reported to be a more methodologically robust method to assess emotional/behavioral problems among children [
62] and was widely used in the clinical settings and community, it was a screening tool after all. It was difficult to use diagnostic instrument to confirm children’s neuropsychological status in the field with large sample size. Currently, researches specifically designed for predictive validity of SDQ in preschoolers on later childhood help seeking in China are limited. When normative data of the Chinese translation of the SDQ were described in a large group of children aged between 3 and 17 years old, researchers had performed validity analysis towards Chinese version of SDQ. It was proved to have favorable cross-scale correlation with the original UK description of the psychometric properties of the SDQ. Convergent validity was acceptable by analyzing between SDQ and PSQ (Conner’s Parent Symptom Questionnaire), and discriminant validity was verified when comparing respondents from the normative sample with ADHD outpatients matched for age and gender [
34]. Predictive validity was testified among some school-aged children in China. It supported the ability of the Chinese SDQ to discriminate between community and clinic children [
63,
64]. Thirdly, we were not able to rule out the potential for residual confounding. For example, parents who requested ECS, especially mothers, may be the same individuals that completed the SDQ. Therefore there might be a rater bias whereby variables that drove the request for ECS in the first place might also drive higher rates of SDQ problems and create an important confound to the current research that limited the ability to draw a link between CS and children’s emotional/behavioral problems. A total of 2455 mothers (74.0%) completed SDQ in our study, which might indicate that ECS on request and SDQ ratings were partly reflective of certain maternal characteristics. It may possibly represent an additional reason for elevated SDQ scores outside the effects of ECS on request. In addition, we didn’t have data on children’s cognitive development and environmental factors such as postnatal corticosteroids exposure and parenting style, as may mediate children’s emotional and social development [
65‐
67]. There might be familial confounding that should be further considered. Based on a population-based sibling design study, Curran EA et al. [
68,
69] had found the relationships between obstetric mode of delivery and autism spectrum disorder and attention-deficit/hyperactivity disorder, which were explained by familial confounding when sibling studies were performed.