Abstract
Background
With the development of assisted reproductive technology, the twinning rate in China has been increasing. However, little is known about twinning from 2014 onwards. In addition, previous studies analysing optimal gestational times have rarely considered maternal health conditions. Therefore, whether maternal health conditions affect the optimal gestational time remains unclear.
Methods
Data of women delivered between January 2012 and December 2020 were collected through China’s National Maternal Near Miss Surveillance System. Interrupted time series analysis was used to determine the rates of twinning, stillbirth, smaller than gestational age (SGA), and low Apgar scores (< 4) among twins in China. To estimate the risk of each adverse perinatal outcome for separate gestational weeks, a multivariate generalised linear model was used. Infants born at 37 weeks of gestational age or foetuses staying in utero were used as reference separately. The analyses were adjusted for the sampling distribution of the population and the cluster effect at the hospital and individual levels were considered.
Results
There were 442,268 infants enrolled in this study, and the adjusted rates for twinning, stillbirth, SGA, and low Apgar scores were 3.10%, 1.75%, 7.70%, and 0.79%, respectively. From 2012 to 2020, the twinning rate showed an increasing trend. Adverse perinatal outcomes, including stillbirth, SGA, and low Apgar scores showed a decreasing trend. A gestational age between 34 and 36 weeks decreased most for rate of stillbirth (average changing rate -9.72%, 95% confidence interval [CI] -11.41% to -8.00%); and a gestational age of between 37 and 38 weeks decreased most for rates of SGA (average changing rate -4.64%, 95% CI -5.42% to -3.85%) and low Apgar scores (average changing rate -17.61%, 95% CI -21.73% to -13.26%). No significant difference in changes in twinning rate or changes of each perinatal outcome was observed during periods of different fertility policies. Infants born at 37 weeks of gestation had a decreased risk of stillbirth, SGA, and low Apgar scores. Maternal antepartum or medical complications increased the risk of SGA and low Apgar scores in different gestational weeks.
Conclusion
China’s twinning rate showed an increasing trend, while adverse perinatal outcomes decreased from 2012 to 2020. Fertility policy changes have had little effect on the twinning rate or the rate of adverse perinatal outcomes such as stillbirth, SGA, or low Apgar scores. The optimal gestational age for twins was 37 weeks. Women pregnant with twins and with antepartum or medical complications should be cautious due to an increased risk of SGA and low Apgar scores.
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Introduction
Since the 1970s, twin births have increased rapidly in developed countries [1]. However, due to an insufficient registration system, the condition of twins is rarely reported in less developed countries. ** countries, has remained constant during 1993–2005 [2]. Deng et al. reported an increasing trend in the Chinese twinning rate from 2007 to 2014 [3]. However, little is known about the trend in twins after 2014. Research has shown that changes in the Fertility policy in 2016, namely, the introduction of the “universal two child policy”, have had an effect on the number of new-born infants. There were 5.4 million new-borns promoted by the new policy, but this change seemed to have little effect on the outcomes of perinatal health [4]. Whether the policy change has had an effect on twin births remains unknown.
Evidence has shown that the relative risk of adverse outcomes may depend on gestational age [5, 6]. Women with a twin pregnancy are more likely to undergo preterm birth, and approximately only half of women will give birth after 37 weeks of gestation [7]. Thus, the optimal gestational age for twin pregnancies may differ from that of singletons. The United Kingdom (UK) clinical guidelines support a policy of elective delivery from 37 weeks 0 days in dichorionic pregnancies (two placentae and two separate chorions) and 36 weeks 0 days in monochorionic pregnancies (one placenta and either one or two chorions) in order to reduce adverse short-term outcomes in twins, such as perinatal mortality [8]. Previous multiple population-based studies have indicated that births delivered between 37 and 39 weeks had the lowest risk of perinatal mortality and morbidity [9, 10]. However, these studies rarely took maternal and perinatal complications into consideration and concluded the “optimal gestational delivery week” specifically on “women with an uncomplicated twin pregnancy” [11, 12]. Whether maternal complications can have an effect on the recommended optimal gestational week is largely unknown. On the other hand, a significant number of twin-analysis research has suffered from small sample sizes and low twinning birth rates, making it difficult to accumulate a large set of twin data. This study, based on China’s National Maternal Near Miss Surveillance System (NMNMSS), collected data from 2012 to 2020, covering 30 provinces of mainland China. The system has helped in policy development and disease burden assessments in both China and worldwide [13,14,35] and higher than in developed countries such as the US (15.8‰, 2005–2006) [36] and the UK (6.16‰ in 2016) [37]. From 2012 to 2020, the stillbirth, SGA, and low Apgar score rates showed decreasing trends. However, the fertility policy has been observed to have little effect on the adverse perinatal outcomes of twins. These parameters may have benefited from China’s social and economic development, and government strategies for strengthening pregnancy health management and improving maternal and neonatal outcomes, such as maternal and foetal physical examinations and health evaluations; referral of women having a high risk pregnancy, equal access to basic public health services, the establishment of near miss new-born care centres, and guidance for the clinical management of twin pregnancies [38, 39]. China’s government made significant efforts to improve maternal and perinatal outcomes by promoting perinatal examinations. The National Basic Public Health Service Project has offered rural pregnant women five times of the perinatal examination appointments for free [40]. Our results showed that 84.17% of the twin infants underwent at least five times prenatal examinations during pregnancies. Infants born with inadequate prenatal examinations (i.e., less than five) had higher risk of stillbirth, SGA, and low Apgar scores. Besides, the National Health Commission of China has promoted health education by popularizing basic health knowledge applicable to women pre-marriage, pre-pregnancy and during pregnancy using several mediums, thereby increasing the knowledge and awareness of health care for women and families. The National Health Commission of China has also organized the “Neonatal Asphyxia Resuscitation Training Program” to reduce the mortality and disability rates of neonatal asphyxia since 2004. The training was first conducted in the “Reducing Maternal Mortality and Eliminating Neonatal Tetanus” program province, and was subsequently expanded to other provinces by offering provincial teacher training, teaching materials, and technical support [41]. Now, the “Neonatal Asphyxia Resuscitation Techniques” have been adopted as a basic skill test for midwives and doctors. Additionally, standardized training of obstetricians during their first three years of practice in China has enhanced the standardization of obstetric practices and the improvement of overall obstetrics technology and service quality.
While the stillbirth, SGA, and low Apgar score rates were on a decreasing trend over the years, the annual decreasing rate for various gestational ages was different, decreasing the most between 37 and 38 weeks. A previous multiple-population based study indicated that births delivered between 37 and 39 weeks had the lowest risk of perinatal mortality and morbidity [9]. However, the “optimal gestational age” rarely considered maternal and perinatal complications [11, 12]. In this study, we classified enrolled women as having uncomplicated pregnancies (including those with maternal health conditions), pregnancies with medical diseases, and pregnancies with antepartum complications. To select the optimum gestational age with the lowest risk of stillbirth, SGA, and a low Apgar score, we used two methods to estimate the risk of each adverse outcome. One was comparing foetuses delivered at different gestational weeks with foetuses delivered at 37 gestational weeks (the conventional method); the other was comparing foetuses delivered at any gestational week with ongoing pregnancies. The latter method was used as a measurement of short-term risk [42]. Using this method of risk estimation, infants born at any time between 37 and 39 gestational weeks were associated with a decreased risk of stillbirth. And in the conventional method, infants born at 37 weeks of gestational age were associated with the lowest risk of stillbirth. Our results for stillbirth were generally consistent with those of previous studies [8, 42]. Our results showed that infants born at around 37 weeks of gestation had the lowest risk of stillbirth, while infants born at shorter or longer gestational ages, especially those born at extremely short gestational ages had higher risks of stillbirth. This is possibly due to twin pregnancies being associated with increased risks of stillbirth and preterm labour. Monochorionic pregnancies negatively affect the in-utero survival of twins, even in monochorionic-diamniotic twins without abnormalities [43]. Monochorionic twins also experience complications like twin to twin transfusion syndrome and selective intrauterine growth retardation. These complications increase the risk of stillbirths. Premature infants have higher risk of stillbirth [44]. Twin pregnancies have higher risk of preterm labour than singleton pregnancies, to the extent that over half of the women pregnant with twins give birth before 37 weeks of gestation [7]. Furthermore, twin pregnancies are generally more likely when using ART [45]. The women who underwent ART were either of advanced age or had declining fertility. It is well-established that advanced age is an independent risk factor for adverse maternal and perinatal outcomes [31]. Women of advanced ages had higher risk of stillbirth. In our results, women with antepartum complications had increased risks of stillbirth when the gestational age was less than 33 weeks. We assumed that these could possibly be a form of natural selection of the implanted embryos to alleviate the additional burden of not successfully sustaining twin pregnancies in women with antepartum complications, leading to stillbirths at an early gestational age. Research has showed that ART-conceived pregnancies were associated with higher risk of birth defects and stillbirths [45, 46]. One study found that in comparison with the gestational ages of stillborn infants of women who conceived spontaneously, the mean gestational age at stillbirth was lower for infants conceived through fertility treatments, suggesting different aetiologies of stillbirth [47]. In addition, we found that live-born twins delivered at a gestational age between 37 and 38 weeks were associated with a lower risk of SGA and low Apgar scores. Furthermore, we found that in reference to uncomplicated pregnancies, women with antepartum complications were associated with an increased risk of giving birth to SGA infants in different gestational weeks compared with ongoing pregnancies. Live-born infants born at any time between 28 and 39 weeks among women with medical diseases, and 28 and 34 weeks among women with antepartum complications were associated with an increased risk of low Apgar scores. Although the increased risk of SGA or low Apgar scores were in accordance with previous research, few of them analysed these associations at different gestational ages [48,49,50,51]. Besides, in subgroup analysis, infants born at 37 or 38 weeks of gestational age were associated with a decreased risk of stillbirth, SGA, and low Apgar score when compared with ongoing pregnancies. Thus suggesting that 37 and 38 weeks were the optimal gestational ages for decreased risk of stillbirth, SGA, and low Apgar scores when compared with ongoing pregnancies.
The strength of this study was in demonstrating the twinning rate and health condition of twins in an adequate sample size from 2012 to 2020 and analysing the health conditions of twins at different gestational ages. However, there are still limitations to this study. Firstly, the weighting method of population distribution may not have been fully adjusted for the oversampling of high-level hospitals when estimating the stillbirth, SGA, and low Apgar rate of twins. Secondly, we could not distinguish whether the twins were monochorionic or dichorionic, and the type of chorionicity was an important factor for stillbirth and perinatal health in twin born infants. Further studies could explore different types of twins.
Conclusions
The twinning rate in China showed an increasing trend from 2012 to 2020, and the adverse perinatal outcomes of twins showed a decreasing trend during the same period. Changes in the fertility policy have little effect on the twinning rate or the rate of adverse perinatal outcomes such as stillbirth, SGA, or rate of low Apgar scores. The optimal gestational age for twins to lower the risk of stillbirth, SGA, and low Apgar scores was 37 weeks. Women with medical diseases or antepartum complications should be more cautious as they have an increased risk of adverse outcomes.
Availability of data and materials
The datasets generated and/or analysed during the current study are not publicly available due to the terms of our contract with the Chinese National Health Commission but are available from the corresponding author on reasonable request.
Abbreviations
- SGA:
-
Small-for-gestation-age
- NMNMSS:
-
National Maternal Near Miss Surveillance System
- ITSA:
-
Interrupted Time Series Analysis
- GLM:
-
Generalised Linear Model
- aORs:
-
Adjusted odds ratios
- CIs:
-
Confidence intervals
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Acknowledgements
The authors acknowledge the institutions and staff of the National Maternal Near Miss Surveillance System for data collection, data entry, and data verification.
Funding
This study was supported by the National Key R&D Program of China (Grant No. 2019YFC1005100), the National Health Commission of the People’s Republic of China, the China Medical Board (Grant No. 11–065), the WHO (Grant No. CHN-12-MCN-004888), and UNICEF (Grant No. 2016EJH016). We thank the institutions and staff of the National Maternal Near Miss Surveillance System for data collection.
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P.C., M.L., J.L., and Y.X. designed the study with contribution from all authors. P.C. and M.Y. did the statistical analysis with support from Z.L., Y.W., X.L, Q.L., J.Z. and L.D., P.C., M.L., J.L., and Y.X. prepared the first draft and all authors contributed to critical interpretation of the results and development of the report. All authors saw and approved the final version.
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This study was approved by the Ethics Review Committee of West China Second University Hospital, Sichuan University, and conducted in accordance with the principles of the Declaration of Helsinki. Because of the retrospective design of this study, the Ethics Review Committee of West China Second University Hospital, Sichuan University has waived the requirement of the informed consent for this study.
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Supplementary Information
Additional file 1:
Supplementary Figure 1. Incidence of stillbirth by year and gestational age.
Additional file 2: Supplementary Figure 2.
Incidence of SGA by year and gestational age.
Additional file 3:
Supplementary Figure 3. Incidence of Low Apgar score by year and gestational age.
Additional file 4: Supplementary Figure 4.
Association between maternal complications and adverse perinatal outcomes in women of advanced ages.* *Foetuses staying in utero were used as reference in separate gestational ages, women in medical diseases group or antepartum complications group were compared with uncomplicated women. All results were adjusted for the sampling distribution of the population and clustered of births within hospitals and pregnant woman individuals. Covariates were adjusted as area classification, geographic location, hospital level, infants birth year, education, marriage, parity, prenatal examination, twins born sequence and weight imbalance.
Additional file 5:
Supplementary Table 1.Risk of stillbirth at Each Week of Gestation Compared with Remaining in Utero categorized by maternal complication condition. Supplementary Table 2.Risk of SGA at Each Week of Gestation Compared with Remaining in Utero categorized by maternal complication condition. Supplementary Table 3.Risk of low apgar score (<4) at Each Week of Gestation Compared with Remaining in Utero categorized by maternal complication condition.
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Chen, P., Li, M., Mu, Y. et al. Temporal trends and adverse perinatal outcomes of twin pregnancies at differing gestational ages: an observational study from China between 2012–2020. BMC Pregnancy Childbirth 22, 467 (2022). https://doi.org/10.1186/s12884-022-04766-0
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DOI: https://doi.org/10.1186/s12884-022-04766-0