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Gestational diabetes complicated with preterm birth: a retrospective cohort study

BMC Pregnancy and Childbirth volume 24, Article number: 631 (2024) Cite this article

Abstract

Objective

To delineate the clinical characteristics of preterm birth (PTB) in the context of gestational diabetes mellitus (GDM).

Methods

A retrospective cohort study was conducted, including 14,314 pregnant women with GDM who delivered at Fujian Provincial Maternity and Children’s Hospital from January 1, 2018, to December 31, 2021. PTB was stratified into late PTB (34–36 weeks of gestation) and early PTB (< 34 weeks) and pregnancy complications were analyzed.

Results

Compared to the term birth (TB) cohort, a higher prevalence of premature rupture of membranes, hypertensive diseases of pregnancy (HDP), intrahepatic cholestasis of pregnancy (ICP), anemia and cervical insufficiency was observed in the PTB cohort. Notably, early PTB increased the incidence of HDP, ICP, anemia and cervical insufficiency compared to late PTB. In the early stages of pregnancy, early PTB was characterized by elevated triglyceride (TG) levels and decreased high-density lipoprotein cholesterol (HDL-C) levels compared to late PTB. In the late pregnancy stages, early PTB was associated with increased white blood cell (WBC) and neutrophil counts. No disparities were observed in 75 g oral glucose tolerance test (OGTT) between early and late PTB.

Conclusion

Enhanced surveillance and management of GDM, particularly in the presence of HDP, ICP and anemia, are imperative to mitigate the risk of PTB. The lipid profile may serve as a predictive tool for early PTB in the early stages of pregnancy, warranting further studies.

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Introduction

Gestational diabetes mellitus (GDM), accounts for approximately 80.3% of cases of gestational hyperglycemia with pregestational diabetes mellitus (PGDM) and impaired glucose tolerance during pregnancy accounting for the remainder [1]. Based on the International Diabetes Alliance report, the global prevalence of GDM was nearly 14% between 2019 and 2021 [2]. A meta-analysis indicated that the prevalence of GDM is approximately 14.8% in mainland China [3]. With the increasing prevalence of obesity, there is a corresponding surge in GDM and its perinatal complications [4].

Preterm birth (PTB) is defined as live birth before 37 weeks of gestation. The diagnostic threshold for PTB varies internationally, being 20 weeks in developed nations and 28 weeks in developing countries, including China [5]. The global PTB rate in 2020 was estimated to be 12%, amounting to 15 million infants born prematurely annually. Among them, 1 million succumb to related complications [6].

Although the risk factors of PTB, such as advanced maternal age, multiple gestations, and male sex of the fetus, are well-documented [7], GDM presents a potentially modifiable and preventable risk factor. Many previous studies have linked GDM with PTB [8,9,10,11,12,13] and a variety of factors have been proposed to explain the link, including maternal hypertension [14], glycemic control [13], oxidative stress [15] and inflammatory factors that are associated with insulin resistance in general and the development of GDM [16]. However, the relationship between GDM and PTB and the mechanisms underlying this association remain to be fully elucidated before a suitable panel of predictive biomarkers may be characterized. The current study aimed to delineate the clinical characteristics of GDM in relation to PTB imposing a gestational time-dependent perspective by focusing on early and late PTB. A retrospective cohort study was conducted and metrics of glycemic control (oral glucose tolerance test), lipidemia (serum lipid profile) and inflammatory status (white blood cell count and composition) recorded with the aim of identifying clinical and biochemical predictors of PTB in women with GDM, thereby establishing strategies for the prevention and management of PTB and its morbidities.

Methods

Study design

This retrospective cohort study was conducted at Fujian Provincial Maternity and Children’s Hospital, enrolling 14,314 pregnant women with singleton pregnancies who were diagnosed with GDM and delivered between January 1, 2018, and December 31, 2021. The participants were stratified into two groups based on the outcome of interest: (1) preterm birth (PTB), which was further categorized into early PTB (less than 34 weeks of gestation) and late PTB (34–36 weeks of gestation), and (2) term birth (TB, 37–42 weeks of gestation). Our primary objective was to analyze and compare the clinical characteristics and pregnancy complications between these groups to achieve a time-dependent profile of factors linking GDM and PTB. In the PTB group, there were 670 pregnant women who underwent regular obstetric checkups at Fujian Provincial Maternity and Children’s Hospital and had complete laboratory information.

Women with GDM who had live singleton births were included. Exclusion criteria were as follows: (1) women with multiple pregnancies; (2) fetal chromosomal abnormalities or structural defects; (3) stillbirth or miscarriage; (4) pregestational diabetes mellitus (PGDM) and unclear diagnosis of GDM and (5) incomplete delivery information. The recruitment process is depicted in Fig. 1.

Data collection

Data were collated through the hospital’s comprehensive electronic medical record system: (1) General information, including maternal age, education level, pre-pregnancy body mass index (BMI), history of miscarriage, parity, mode of conception and the method of delivery; (2) Pregnancy complications, such as premature rupture of membranes (PROM), hypertensive disorders of pregnancy (HDP), intrahepatic cholestasis of pregnancy (ICP), anemia, thyroid disorders, uterine scar, uterine fibroids, uterine malformations, cervical insufficiency, breech presentation, fetal distress, polyhydramnios, oligohydramnios, placenta previa or placenta accreta, placental abruption and postpartum hemorrhage; (3) Laboratory parameters, including fasting plasma glucose (FPG), white blood cell (WBC) count, hemoglobin (HGB) level, neutrophil (NEUT) count, platelet (PLT) count, triglyceride (TG) level, total cholesterol (TC) level, high-density lipoprotein cholesterol (HDL-C) level, low-density lipoprotein cholesterol (LDL-C) level and results of the 75 g oral glucose tolerance test (OGTT) at 0, 1, and 2 h.

Diagnostic criteria

The diagnosis of the disease was based on the 10th edition of the International Classification of Diseases (ICD-10). According to China’s “Guidelines for the Diagnosis and Treatment of Hyperglycemia in Pregnancy (2022)“ [17], a 75 g oral glucose tolerance test (OGTT) was performed between the 24th and 28th weeks of pregnancy with the diagnostic cutoff values for OGTT at 0 h, 1 h and 2 h being 5.1 mmol/L, 10.0 mmol/L and 8.5 mmol/L, respectively. The lower limit for preterm birth was chosen based on China’s “Clinical Diagnosis and Treatment Guidelines for Preterm Birth“ [5], delivery before 37 weeks and after 28 weeks of pregnancy. Classification standards were selected based on the 25th edition of “Williams Obstetrics“ [18], preterm birth before 34 weeks of gestation was considered early PTB and preterm birth between 34 and 36 weeks of gestation was considered late PTB.

The whole course of pregnancy was divided into three periods. Before the end of the 13th week of pregnancy was considered early pregnancy; between the end of the 14th and 27th week was considered mid-pregnancy and the 28th week and thereafter was considered late pregnancy.

Statistical analysis

Statistical analyses were performed using SPSS 26.0 software. Categorical data are presented as frequencies, percentages or rates. Comparisons were conducted using the chi-square test or Fisher’s exact test, where appropriate. We employed the Kolmogorov‒Smirnov test to confirm data normal distribution. Continuous data conforming to normal distribution are expressed as mean ± standard deviation (SD). Such data were compared using the independent samples t-test. Non-normally distributed continuous data are presented as median (25th to 75th percentile) [M(P25 ~ P75)]. For non-normal data, differences were assessed using the Mann-Whitney U test. A two-sided P-value of less than 0.05 was considered statistically significant. A total of 670 cases of pregnant women who regularly attended prenatal check-ups and had early laboratory data at our hospital were identified, although some information was still incomplete. We addressed the missing data by employing median imputation for the cultural level of the pregnant women and regression imputation for their pre-pregnancy BMI; the remaining indicators were complete.

Fig. 1
figure 1

Flowchart of the study population. Footnotes HIP: Hyperglycemia in pregnancy; GDM: Gestational diabetes mellitus; PGDM: Pregestational diabetes mellitus; TB: Term birth; PTB: Preterm birth

Full size image

Results

This study comprised 14,314 pregnant women with GDM who delivered at Fujian Provincial Maternity and Children’s Hospital from January 1, 2018, to December 31, 2021. The incidence of PTB among these women was 8.55% (1,224 cases). Early PTB and late PTB occurred for 2.33% (334 cases) and 6.22% (890 cases) of the participants, respectively.

Demographic and clinical characteristics were compared between women with PTB and those with TB. Women with PTB were more likely to have advanced maternal age, a history of several pregnancies or a history of miscarriage (P < 0.05). There was no significant difference in the use of assisted reproductive technology (ART) between the PTB and TB groups (P > 0.05). Pregnancy complications were more prevalent in the PTB group compared to the TB group, including PROM, HDP, ICP, anemia, uterine fibroids, uterine malformations, cervical insufficiency, breech presentation, placenta previa or placenta accreta and placental abruption (P < 0.05). The rates of cesarean section and postpartum hemorrhage were also significantly higher in the PTB group (P < 0.05). These findings are summarized in Table 1.

Table 1 Demographic and clinical characteristics of women with and without PTB in GDM
Full size table

Compared with late PTB, women with early PTB had a higher average pre-pregnancy BMI, were more likely to have a history of miscarriage and more often needed insulin during pregnancy (P < 0.05). The incidence of PROM was lower in early PTB compared to late PTB, whereas HDP, ICP, anemia, cervical insufficiency, breech presentation, placental abruption and chorioamnionitis were more common in early PTB (P < 0.05). There were no significant differences in the rates of cesarean section and postpartum hemorrhage between the early and late PTB groups (P > 0.05) (Table 2).

Table 2 Demographic and clinical characteristics of women with different severity of PTB in GDM
Full size table

We compared laboratory parameters between 129 cases with early PTB and 541 cases with late PTB who regularly attended prenatal check-ups at our hospital and had complete laboratory information during the whole pregnancy period. Women with early PTB had significantly lower levels of HDL-C and higher levels of TG in the early pregnancy period compared to those with late PTB (P < 0.05). In the late pregnancy period, early PTB was associated with higher WBC and NEUT counts (P < 0.05). There were no significant differences in FPG and 75 g OGTT results between the two subgroups of PTB (P > 0.05) (Tables 3, 4 and 5).

Table 3 Comparison of laboratory tests in early pregnancy in GDM
Full size table
Table 4 Comparison of laboratory tests in mid-pregnancy in GDM
Full size table
Table 5 Comparison of laboratory tests in late pregnancy in GDM
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Discussion

The current retrospective cohort study gives an overview of the clinical characteristics of PTB in women with GDM. We found that the proportion of women with GDM in the early PTB group who had a college degree or above (more than 12 years of education) was lower than that in the late PTB group. Women with GDM and lower education levels are mostly engaged in physical labor, have insufficient income and medical insurance coverage, lack knowledge about reproductive health and perinatal care, and have poor compliance and poorly controlled blood sugar, factors which are considered to lead to preterm birth among the general population [19, 20]. High pre-pregnancy BMI has been considered a risk factor for spontaneous PTB [21], and medically indicated PTB is associated with a BMI > 40 kg/m² [22]. The current cohort of GDM patients with early PTB had a higher pre-pregnancy BMI than those with late PTB, illustrating that the association of PTB with GDM and its risk factors extends to a time-dependent relationship with gestational progress. The contribution of higher pre-pregnancy leptin levels in women with higher BMIs warrants further investigation and the influence of leptin levels on fetal size has been indicated previously [23], although the situation concerning any role of leptin in pregnancy and labor is complicated by the contribution to serum levels by placental production. Many studies have demonstrated that advanced maternal age increases the risk of preterm birth [24] and this finding was supported by the current cohort, although no link was found between higher maternal age and early PTB. It has been observed that recurrent GDM amplifies the incidence of preterm birth among multiparous women with a history of pre-pregnancy obesity, contrasting with those affected by GDM in the current gestation alone [25]. This pronounced effect is posited to stem from the interplay between obesity and a spectrum of metabolic and immunological dysregulations, including hyperinsulinemia, insulin resistance, and chronic inflammation of the placenta, as delineated in previous studies [26].

Consistent with previous studies [27,28,29], our findings indicated that HDP, ICP, and anemia are associated with preterm birth. Previous studies have reported the association between GDM and pregnancy complications, including HDP and ICP [30]. These conditions can contribute to PTB, potentially through shared pathophysiological mechanisms involving inflammation and oxidative stress. In this study, we observed a higher incidence of pregnancy complications, such as placenta previa and placenta accrete, in the PTB group. The rates of cesarean section and postpartum hemorrhage were also higher in the PTB group, possibly because placenta previa and placenta accreta were risk factors for medically indicated PTB. Our results highlight the need for vigilant monitoring and proactive management of GDM to mitigate the risk of PTB and its morbidities.

Interestingly, our study revealed that in early pregnancy, there were lower HDL-C levels and higher TG levels in the early PTB group compared to the late PTB group and this change in serum lipid profile has been linked to the development of a proinflammatory state and increased levels of C-reactive peptide [31]. Abnormal lipid metabolism may be a factor in inducing PTB. Cholesterol is essential for placental angiogenesis while hyperlipidemia induces inflammation and oxidative stress. Increased levels of total cholesterol, triglycerides and HDL-C were associated with PTB and hyperlipidemia may be a risk factor, independent of mothers’ pre-pregnancy BMI or weight [32]. Mudd et al. [33]. found reduced concentrations of TC, LDL-C and HDL-C to be correlated with moderately elevated risk of medically indicated preterm births and elevated levels of TC, LDL-C, and triglycerides are observed to be associated with an increased likelihood of spontaneous preterm births. Wang et al. [34] found that insulin resistance is the primary cause of increased TG levels and decreased HDL levels in pregnant women with GDM. In addition, there was a significant correlation between the TG/HDL ratio and the prevalence of GDM. Dysregulated serum lipid profiles and elevated levels of pro-inflammatory cytokines have been associated with a state of oxidative stress in many pathological conditions, including gestational insulin resistance and GDM [35, 36]. A state of maternal oxidative stress may be linked to free radical damage to fetal tissues given the limited anti-oxidant defenses of the fetus and thus contribute to some of the observed adverse outcomes associated with GDM. The early PTB group had higher WBC and NEUT levels compared to the late PTB group in late pregnancy and this is further confirmation of a greater pro-inflammatory state among the early PTB patients. A retrospective cohort study from a tertiary hospital in China [37] assessed the relationship between WBC and adverse outcomes during pregnancy. Among patients with GDM, increased WBC count elevated the risk of adverse pregnancy outcomes in the first trimester (adjusted ORs (aOR) 1.06 (95% CI, 1.00-1.13)) and second trimester (aOR 1.10 (95% CI, 1.04–1.16)). Among patients with PTB, increased WBC count elevated the risk of adverse pregnancy outcomes in the first trimester (aOR 1.12 (95% CI, 1.06–1.18)), second trimester (aOR 1.10 (95% CI, 1.06–1.13)), and third trimester (aOR 1.12 (95% CI, 1.09–1.15)). The current work indicates that elevated lipid levels in the early stages of GDM pregnancy may be associated with an increased inflammatory burden and also may be related to PTB but the specific mechanisms underlying this relationship require further investigation.

Ding et al. [38] found elevated FPG level in pregnant women with GDM to be significantly associated with PTB and a study from northwest China [39] indicated that each 1 mmol/L increase in FPG increased the risk of PTB. The potential biological link between glucose levels and PTB may involve inflammatory pathways that can affect the placenta and vascularization [40, 41], and high maternal blood glucose is also likely to increase the risk of early delivery due to fetal macrosomia causing the fetus to grow large for gestational age [42]. However, the current study did not find differences in FPG or in 1–2 h values following the OGTT among different categories of preterm birth. Blood glucose levels are known to fluctuate during pregnancy and further studies are needed to clarify the relationship between blood glucose values in women with GDM and preterm birth. It has also been suggested that GDM causes unusual methylation patterns in fetal DNA and fetal contributions to early onset of labor and preterm birth cannot be ignored although this area falls outside the scope of the current work [43, 44].

It is important to acknowledge the limitations inherent to the retrospective design of our study which may introduce information and selection bias. The current study population may also produce findings that are not generalizable to groupings of different ethnicity. There are many other factors with an influence on GDM and pregnancy, such as pursuit of physical activity, dietary practices, pre-pregnancy BMI changes and smoking or alcohol consumption which are potential co-variates. These factors were outside the scope of the present study but warrant further investigation.

Conclusions

In conclusion, our study revealed that in patients with GDM, the incidence of other complications of pregnancy was higher in the PTB group than in the TB group. Furthermore, the incidence of other complications of pregnancy in the early PTB group was higher than that in the late PTB group. To prevent PTB and, especially, early PTB, it is necessary to enhance the management of GDM complicated by HDP, ICP, anemia, and other pregnancy complications. In the early stages of pregnancy, there is a difference in the lipid profile between early PTB and late PTB. Tight control of blood lipids in GDM may effectively prevent early preterm birth.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

ART:

Assisted reproductive technology

BMI:

Body mass index

FPG:

Fasting plasma glucose

GDM:

Gestational diabetes mellitus

HDL-C:

High-density lipoprotein cholesterol

HDP:

Hypertensive disorders in pregnancy

HGB:

Hemoglobin

ICP:

Intrahepatic cholestasis of pregnancy

LDL-C:

Low-density lipoprotein cholesterol

NEUT:

Neutrophil count

OGTT:

Oral glucose tolerance test

PGDM:

Pregestational diabetes mellitus

PLT:

Platelet count

PROM:

Premature rupture of membranes

PTB:

Preterm birth

TB:

Term birth

TC:

Total cholesterol

TG:

Triglyceride

WBC:

White blood cell

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Acknowledgements

We would like to express our gratitude to EditSprings (https://www.editsprings.cn) for the expert linguistic services provided.

Funding

This study was supported by Joint Funds for the innovation of Science and Technology, Fujian province, [2020Y9134] and Innovation Platform Project of Science and Technology, Fujian province [2021Y2012]. The funding source 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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Authors and Affiliations

  1. Fujian Provincial Maternity and Children’s Hospital, No. 18, Daoshan Road, Gulou District, Fuzhou, Fujian Province, 350001, China

    Shuyao Huang, Yanni Guo, Xia Xu, Lingling Jiang & Jianying Yan

  2. College of Clinical Medicine for Obstetrics & Gynecology and Pediatrics, Fujian Medical University, Fuzhou, China

    Shuyao Huang & Jianying Yan

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  1. Shuyao Huang
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Contributions

All authors contributed to manuscript editing and read and approved the final manuscript. Shuyao Huang and Xia Xu contributed to the study design. The analysis was made by Shuyao Huang in discussion and with the assistance of Xia Xu and Yanni Guo. Shuyao Huang drafted the manuscript. Xia Xu, Lingling Jiang and Jianying Yan revised of the manuscript.

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Correspondence to Jianying Yan.

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Ethics approval and consent to participate

This study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Ethics Committee of Fujian Provincial Maternity and Children’s Hospital (No. 2020–2049). The requirement for informed consent was waived by the Ethics Committee of Fujian Provincial Maternity and Children’s Hospital because of the retrospective nature of the study.

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Huang, S., Guo, Y., Xu, X. et al. Gestational diabetes complicated with preterm birth: a retrospective cohort study. BMC Pregnancy Childbirth 24, 631 (2024). https://doi.org/10.1186/s12884-024-06810-7

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BMC Pregnancy and Childbirth

ISSN: 1471-2393

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