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The association of early pregnancy dyslipidemia with preterm birth in twin pregnancies: a retrospective cohort study

BMC Pregnancy and Childbirth volume 24, Article number: 616 (2024) Cite this article

Abstract

Background

Maternal lipid metabolism has been implicated in elevating the risk of adverse pregnancy outcomes, which is a particularly significant concern in twin pregnancies. However, the precise relationship between early pregnancy dyslipidemia and the risk of preterm birth (PTB) in twin pregnancies remains unclear.

Methods

This retrospective cohort study included women with twin pregnancies between January 2018 and December 2023. Early pregnancy blood lipid profiles, including total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), triglyceride (TG) and high-density lipoprotein cholesterol (HDL-C), were examined. Dyslipidemia was diagnosed based on the diagnostic criteria outlined in the 2016 guidelines for the prevention and treatment of dyslipidemia in Chinese adults. PTB was defined as birth occurring before 37 weeks of pregnancy. Logistic regression models were used to evaluate the association of early pregnancy dyslipidemia with PTB in twin pregnancies.

Results

A total of 613 women with twin pregnancies were included, and 141 women were complicated with dyslipidemia. The incidence of PTB < 37 weeks was significantly higher in the dyslipidemia group compared to the group without dyslipidemia (64.5% vs. 50.4%, P = 0.003). After adjusting for confounding factors, dyslipidemia was positively associated with PTB < 37 weeks (adjusted odds ratio: 1.71; 95% confidence interval: 1.13–2.58). However, these associations varied depending on the chorionicity and mode of conception of the twins. The positive associations between early pregnancy dyslipidemia and PTB < 37 weeks remained significant only in spontaneously conceived (SC) or dichorionic diamniotic (DCDA) twin pregnancies. No statistically significant associations were observed between dyslipidemia and the other secondary outcomes.

Conclusion

Early pregnancy dyslipidemia was positively associated with PTB < 37 weeks in twin pregnancies, and this association remained significant in SC or DCDA twin pregnancies. Comprehensive lipid profile assessment in the first trimester may be beneficial for patients’ monitoring and implementing interventions to mitigate adverse pregnancy outcomes.

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Background

Blood lipids are a diverse group of fat-like substances present in the bloodstream, playing crucial roles in cellular structure and energy storage. These include cholesterol, triglycerides, phospholipids, and lipoproteins [1]. Lipids are essential for maintaining overall health, but imbalances can lead to various health issues, including cardiovascular disease, metabolic syndrome, and other related conditions [2, 3]. During pregnancy, maternal serum lipid levels naturally increase, making pregnant women more susceptible to dyslipidemia [4]. Dyslipidemia during pregnancy can significantly impact both maternal and fetal health, potentially leading to adverse outcomes such as gestational diabetes mellitus (GDM), preterm birth (PTB), and other complications in singleton pregnancies [5,6,7]. Unfortunately, the lack of established guidelines for lipid reference ranges during pregnancy complicates the situation, and the scarcity of safety data is a significant barrier to developing effective treatments for managing gestational dyslipidemia.

Twin pregnancies carry a higher perinatal risk compared to singleton pregnancies due to increased metabolic demands and a range of physiological, genetic, and environmental factors that elevate the likelihood of complications for both the mother and the babies [8,9,10]. Preterm birth, defined as delivery before 37 weeks of gestation, is significantly more common in twin pregnancies [11]. This may be due to the increased uterine burden and heightened competition between twins [12]. Several other factors also contribute to the elevated perinatal risks in twin pregnancies [13]. While some studies have explored the association between lipid levels and the risk of PTB in singleton pregnancies, findings vary regarding which lipid components are implicated and the strength of these associations [6, 14]. A significant knowledge gap remains concerning the impact of dyslipidemia on PTB specifically in twin pregnancies.

Hence, this study aims to fill this gap by investigating the association between early pregnancy dyslipidemia and PTB in twin pregnancies, while also exploring potential variations based on chorionicity or mode of conception. By elucidating these aspects, we aspire to provide valuable insights for clinical practice, offering opportunities to refine the management and outcomes of twin pregnancies.

Materials and methods

Study design and population

This retrospective cohort study took place at Sichuan Jinxin Xinan Women and Children’s Hospital in southwest China, covering the period from January 2018 to December 2023. A total of 1555 women with twin pregnancies were initially included in the study. Consistent with previous studies [15], dyslipidemia was defined by meeting one or more of the following criteria: total cholesterol (TC) ≥ 6.22 mmol/L (240 mg/dl), low-density lipoprotein cholesterol (LDL-C) ≥ 4.14 mmol/L (160 mg/dl), high-density lipoprotein cholesterol (HDL-C) < 1.04 mmol/L (40 mg/dl), and triglyceride (TG) ≥ 2.26 mmol/L (200 mg/dl). Participants were excluded if they had pre-existing metabolic diseases before pregnancy (n = 22), monochorionic monoamniotic (MCMA) twin pregnancies (n = 1), unknown chorionicity (n = 33; chorionicity was determined by first-trimester ultrasound, which assessed the presence of two distinct chorions, the positive lambda sign, and the number of placental masses) [16], stillbirth (n = 6) or incomplete blood lipid data (n = 880). After these exclusions, the final cohort consisted of 613 women with twin pregnancies, including 472 without dyslipidemia and 141 with dyslipidemia. The study received approval from the Ethics Committee of Sichuan Jinxin Xinan Women and Children’s Hospital (No. 2021014) and the Ethics Committee of Chongqing Medical University (No. 2021060).

Data collection and outcomes

We collected data from the hospital’s electronic medical record system, including maternal baseline characteristics, pregnancy complications, obstetric outcomes, and neonatal birth weight and gestational age, as previously detailed [17, 18]. The primary outcome was PTB < 37 weeks. This was further divided into several categories: PTB < 34 weeks, spontaneous preterm birth (sPTB), and iatrogenic preterm birth (iPTB). sPTB resulted from premature rupture of membranes, while iPTB resulted from other medical interventions, such as labor induction or cesarean section [19]. Other secondary outcomes included a range of pregnancy and neonatal outcomes. Small for gestational age (SGA) was defined as a birth weight below the 10th percentile for gestational age and sex, while low birth weight (LBW) was characterized by a birth weight below 2500 g at delivery. Birth weight discordance was determined using the formula: (birth weight larger twin - birth weight smaller twin) / birth weight larger twin × 100, with a threshold of 20% used to define significant discordance [20]. A low Apgar score was below 7 on the Apgar scale. Among twins, SGA, LBW, or a low Apgar score applied if at least one met the criteria.

Statistical analysis

All statistical analyses were conducted using SPSS software (version 27.0, IBM, USA). The Shapiro-Wilk test and Q-Q plot were utilized to assess the normality of the data. Following normality testing, all continuous variables were approximately normally distributed. The results were presented as mean ± standard deviation (SD) and compared using the Student’s t-test. Categorical variables were expressed as numbers (percentages) and compared using the Chi-square test or Fisher’s exact test. We used multivariable logistic regression to calculate the adjusted odds ratio (OR) and 95% confidence interval (CI). The adjusted variables included: (1) those with statistically significant differences in baseline comparison, and (2) variables that, although not statistically significant in baseline comparison (such as maternal age), are clinically relevant to the outcome variable [17]. Furthermore, attributable risk (AR), attributable risk percentage (AR%), population attributable risk (PAR), and population attributable risk percentage (PAR%) were computed to enhance the primary findings. Power analysis was conducted using PASS software (NCSS, LLC, Kaysville, UT), considering the sample size, significance level (α = 0.05), and relevant regression parameters [21]. The power for the primary outcome of PTB < 37 weeks was calculated to be 83.2%. A P-value < 0.05 was considered statistically significant.

Results

Baseline characteristics

Among the 613 women with twin pregnancies, 472 (77.0%) did not present with dyslipidemia, while 141 (23.0%) presented with dyslipidemia. The baseline comparison between the two groups was presented in Table 1. Twin-pregnant women with dyslipidemia had a significantly higher pre-pregnancy body mass index (BMI) (22.90 kg/m2 vs. 21.54 kg/m2), BMI after admission (28.86 kg/m2 vs. 27.72 kg/m2) and fasting blood glucose (4.65 mmol/L vs. 4.53 mmol/L) than those without dyslipidemia (all P < 0.05). Compared with those without dyslipidemia, the dyslipidemia group exhibited a higher proportion of dichorionic diamniotic (DCDA) (95.7% vs. 89.8%) twins, pregnancies conceived via assisted reproductive technology (ART) (83.0% vs. 72.2%) and gestational diabetes (37.6% vs. 28.6%) (all P < 0.05). The other baseline characteristics showed no statistically significant difference between the dyslipidemia group and the group without dyslipidemia.

Table 1 Baseline characteristics between the two groups
Full size table

Pregnancy and neonatal outcomes

The comparison of pregnancy and neonatal outcomes was presented in Table 2. The overall rate of PTB < 37 weeks in twin pregnancies was 53.7%. The incidence of PTB < 37 weeks was significantly higher in the dyslipidemia group compared to the group without dyslipidemia (64.5% vs. 50.4%, P = 0.003). Similarly, the incidence of iPTB < 37 weeks was significantly higher in the dyslipidemia group compared to the group without dyslipidemia (48.9% vs. 36.9%, P = 0.010). No statistically significant differences were observed in other pregnancy and neonatal outcomes between the dyslipidemia group and the group without dyslipidemia (all P > 0.05).

Table 2 Comparison of pregnancy and neonatal outcomes between the two groups
Full size table

Association of dyslipidemia with pregnancy and neonatal outcomes

The results of univariate logistic analysis indicated a significantly increased risk of PTB < 37 weeks (unadjusted OR: 1.79; 95% CI: 1.21–2.64) and iPTB < 37 weeks (unadjusted OR: 1.64; 95% CI: 1.12–2.40) in the dyslipidemia group compared to the group without dyslipidemia. After adjusting for potential confounding factors, there remained a positive association between dyslipidemia and PTB < 37 weeks (adjusted OR: 1.71; 95% CI: 1.13–2.58) and iPTB < 37 weeks (adjusted OR: 1.59; 95% CI: 1.07–2.38). However, no statistically significant association was observed between dyslipidemia and other secondary outcomes in both univariate and multivariate logistic analyses (Table 3).

Table 3 Association of dyslipidemia with pregnancy and neonatal outcomes
Full size table

Association of dyslipidemia with PTB < 37 weeks stratified by mode of conception and chorionicity

Table 4 showed the results of stratified analyses by mode of conception and chorionicity. The positive associations between dyslipidemia and PTB < 37 weeks remained statistically significant in spontaneously conceived (SC) (adjusted OR: 2.87; 95% CI: 1.02–8.02) and DCDA twin pregnancies (adjusted OR: 1.79; 95% CI: 1.17–2.74). However, no statistically significant associations were found in twin pregnancies conceived through ART or in monochorionic diamniotic (MCDA) twin pregnancies. Univariate analysis revealed a statistically significant association between dyslipidemia and PTB < 37 weeks in twin pregnancies conceived through ART (unadjusted OR:1.60; 95% CI: 1.04–2.46). However, this association was not statistically significant after adjusting for confounding factors.

Table 4 Association of dyslipidemia with PTB < 37 weeks stratified by mode of conception and chorionicity
Full size table

Effect estimation indicators calculated based on the incidence of PTB < 37 weeks

To provide a more comprehensive understanding of the disease prevention and public health significance of the study, the results of calculating AR, AR%, PAR, and PAR% based on the incidence of PTB < 37 weeks were as follows: AR = 14.1%, AR% = 21.9%, PAR = 8.3%, PAR% = 14.1%, respectively (Table 5).

Table 5 Effect estimation indicators calculated based on the incidence of PTB < 37 weeks
Full size table

The AR value of 14.1% indicated that the proportion of PTB < 37 weeks in the dyslipidemia group increased by 14.1% compared to the group without dyslipidemia. If dyslipidemia were eliminated, the incidence of PTB < 37 weeks in twin pregnancies with dyslipidemia could potentially be reduced by 14.1%. The AR% was 21.9%, suggesting that 21.9% of preterm births in twin pregnancies with dyslipidemia may be attributed to dyslipidemia. According to reports [22], PTB < 37 weeks occurs in approximately 58.7% of all twin pregnancies. Therefore, the PAR was 8.3%, indicating that if dyslipidemia were eliminated, the incidence of PTB in women with twin pregnancies could potentially be reduced by 8.3%. The PAR% was 14.1%, suggesting that 14.1% of preterm births in all twin pregnancies may be attributed to dyslipidemia.

Discussion

During pregnancy, maternal serum lipid levels naturally rise as part of the body’s adaptation to support fetal development. This physiological increase is essential for meeting the heightened energy and nutritional demands of both the mother and the fetus [23]. However, this natural elevation in lipid levels can also predispose pregnant women to dyslipidemia, a condition characterized by abnormal levels of lipids in the blood, such as cholesterol and triglycerides. While the impact of dyslipidemia has been extensively studied in singleton pregnancies, where it is recognized as a contributing factor to complications like GDM, PTB, and preeclampsia, its effects in twin pregnancies remain less well understood [5, 6, 14]. Through a retrospective cohort study, we investigated the influence of early pregnancy dyslipidemia on PTB in twin pregnancies. Our findings revealed a significant association between dyslipidemia in the first trimester and PTB < 37 weeks. These results underscore the importance of considering dyslipidemia as a potential etiological factor for PTB in twin pregnancies and suggest its use as a marker for elevated risk. Moreover, our study advocates for a comprehensive assessment of lipid profiles in the first trimester to facilitate early interventions aimed at mitigating adverse pregnancy outcomes.

Studies have shown that, compared to dichorionic (DC) twin pregnancies, monochorionic (MC) twin pregnancies are more prone to preterm delivery and have higher rates of neonatal morbidity and mortality [24]. Lin et al. [19] reported that in vitro fertilization/intracytoplasmic sperm injection (IVF/ICSI) conceived DCDA twins had a higher incidence of PTB < 37 weeks. In our study, after stratifying twin pregnancies by mode of conception and chorionicity, we found a positive association between dyslipidemia and PTB < 37 weeks specifically in SC and DCDA twin pregnancies. One possible explanation is that MCDA twin pregnancies carry a higher risk of multiple adverse outcomes. Compared to DCDA twin pregnancies, MCDA twin pregnancies are typically delivered at an earlier gestational age due to various medical indications [9, 25]. Furthermore, we observed that the proportion of twin pregnancies achieved through ART was higher in the dyslipidemia group compared to the group without dyslipidemia. The increased awareness of prenatal care among the assisted reproductive population might mitigate the adverse effects of dyslipidemia on PTB.

The biological mechanisms linking dyslipidemia with PTB in twin pregnancies could be considered from several perspectives. Maternal lipid metabolism plays a crucial role in pregnancy outcomes, with dyslipidemia elevating the risk of adverse effects, particularly in twin pregnancies due to increased metabolic demands [26]. Hyperlipidemia is known to induce inflammation and oxidative stress [27, 28], which exacerbates the already heightened metabolic burden in twin pregnancies. This inflammatory state is a notable risk factor for PTB [29], potentially explaining the observed association between dyslipidemia and PTB < 37 weeks in SC and DCDA twin pregnancies. In SC twin pregnancies, the maternal adaptation to the placenta is often suboptimal. Dyslipidemia can lead to inadequate placental blood flow and increased inflammation, thereby raising the risk of PTB. In contrast, twin pregnancies conceived through ART benefit from close monitoring and management, which may reduce this risk. Additionally, in DCDA twin pregnancies, where each fetus has a separate placenta, dyslipidemia could impair placental function for each fetus individually. This can result in placental dysfunction and restricted fetal growth [26], thereby increasing the risk of PTB.

The management of lipid abnormalities during pregnancy has become more challenging due to several factors, including the absence of reference ranges for gestational lipid levels, limited evidence from clinical trials, and insufficient data on the effectiveness and safety of lipid-lowering drugs in treating pregnancy complications [30]. However, many studies have established a clear association between dyslipidemia and adverse pregnancy outcomes, such as PTB [6, 14]. Dyslipidemia may be alleviated with lifestyle changes and pharmacological treatments [31]. Early detection and management of dyslipidemia could serve as an indicator for targeted interventions, providing a crucial opportunity to improve outcomes for both mothers and infants. Furthermore, our research highlights the need for tailored dietary and exercise interventions to address dyslipidemia in pregnant women, particularly with twin pregnancies, who face unique metabolic challenges.

Our study has several strengths. Firstly, it is among the first to specifically investigate the association between early pregnancy dyslipidemia and PTB in twin pregnancies. This novel focus fills a critical gap in the literature and provides new insights into how dyslipidemia affects this high-risk population. Secondly, we gathered comprehensive information on pregnancy complications, including gestational hypertension, preeclampsia, and gestational diabetes, which are potential risk factors for adverse pregnancy and neonatal outcomes [32, 33]. These were considered as confounding factors. Finally, to account for the influence of chorionicity and mode of conception, we also conducted a stratified analysis.

However, several limitations should be considered. The single-center, regression-based design may introduce selection and information bias. Additionally, due to the observational nature of our study, we were unable to establish a definitive cause-and-effect relationship. Blood lipid profiles were assessed only in the first trimester, potentially overlooking the dynamic changes throughout pregnancy. It is important to investigate how lipid profiles change over time during pregnancy and their effects on pregnancy outcomes. Therefore, future research should involve larger sample sizes and well-designed prospective multicenter studies to validate our findings and to better understand the complex relationship between dyslipidemia and adverse pregnancy outcomes in twin pregnancies.

Conclusions

In twin pregnancies, early pregnancy dyslipidemia may be positively associated with the rate of PTB < 37 weeks and iPTB < 37 weeks. The relationship between dyslipidemia and PTB < 37 weeks varies based on chorionicity and mode of conception. Therefore, if dyslipidemia is present in early pregnancy, closer monitoring and management may be necessary.

Data availability

The data used and analyzed during the current study are available from the corresponding author upon request.

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Acknowledgements

We are grateful to acknowledge all the participants of this study and the medical staff for their contribution to this work.

Funding

This work received partial support from the National Key Research and Development Program of China (no. 2023YFC2705900).

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Author notes

  1. Li-Yang Zhou and Zhou Xu contributed to the work equally and should be regarded as co-first authors.

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Women and Children’s Hospital of Chongqing Medical University, No.120, Longshan Rd, Chongqing, 401147, China

    Li-Yang Zhou, Li Wen, Xin-Zhen Chen, Ying-Ling Yao, Rui-Ling Liu, Yong-Jia Zhang, Gong-Li Chen & Yu-Bin Ding

  2. Joint International Research Laboratory of Reproduction and Development of the Ministry of Education of China, School of Public Health, Chongqing Medical University, Chongqing, 400016, China

    Li-Yang Zhou, Ying-Ling Yao, Rui-Ling Liu, Yong-Jia Zhang, Zhao-Hui Zhong & Li-Juan Fu

  3. The Department of Obstetrics, Sichuan Jinxin Xinan Women and Children’s Hospital, Chengdu, 610011, Sichuan, China

    Zhou Xu

  4. Department of Pharmacology, Academician Workstation, Changsha Medical University, Changsha, 410219, China

    Li-Juan Fu & Yu-Bin Ding

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Contributions

LYZ and ZX drafted the original manuscript. LYZ and YLY conducted data analysis. YBD and GLC participated in the project design and manuscript revision. LJF provided language revision for the manuscript. ZHZ, RLL and YJZ were involved in the data collection and manuscript revision. XZC and LW provided clinical consultation and assisted in data collection.

Corresponding authors

Correspondence to Gong-Li Chen or Yu-Bin Ding.

Ethics declarations

Ethics approval and consent to participate

The study received approval from the Ethics Committee of Sichuan Jinxin Xinan Women and Children’s Hospital (No. 2021014) and the Ethics Committee of Chongqing Medical University (No. 2021060). The patients provided their written informed consent to participate in this study.

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Not applicable.

Competing interests

The authors declare no competing interests.

Role of the funder/sponsor

The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

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Zhou, LY., Xu, Z., Wen, L. et al. The association of early pregnancy dyslipidemia with preterm birth in twin pregnancies: a retrospective cohort study. BMC Pregnancy Childbirth 24, 616 (2024). https://doi.org/10.1186/s12884-024-06789-1

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BMC Pregnancy and Childbirth

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