High TG/HDL-C ratio suggests a higher risk of gestational diabetes mellitus in the first trimester

doi:10.21203/rs.3.rs-4706362/v1

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High TG/HDL-C ratio suggests a higher risk of gestational diabetes mellitus in the first trimester

https://doi.org/10.21203/rs.3.rs-4706362/v1

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Objective: To investigate the relationship between triglyceride/high-density lipoprotein cholesterol (TG/HDL-C) ratio and gestational diabetes mellitus (GDM) in the first trimester.

Method(s): We followed 2,356 pregnant women who visited the obstetric outpatient clinic of Shanghai General Hospital and underwent regular obstetric examinations from October 1st, 2019 to June 1st, 2021. A 75 g oral glucose tolerance test (OGTT) was performed, and lipid levels were measured in the first trimester. Logistic regressionand restricted cubic spline (RCS) were applied to evaluate the association between the TG/HDL-C ratio and GDM.

Result(s): Among 2,356 pregnant women, 425 women(18.04 %) were diagnosed with GDM. Logistic regression analysis showed that the TG/HDL-C ratio was an independent risk factor for GDM (OR=1.37 (95% CI: 1.16-1.62), p<0.001). After adjusting for potential confounding factors, we observed that a high TG/HDL-C ratio promoted GDM (OR: 1.65, 95% CI: 1.27–2.13, p<0.001). The RCS analysis revealed a signifcant nonlinear association. (P-interaction < 0.05).

Conclusion(s): In this study, we found a significant correlation between TG/HDL-C ratio and GDM, and high TG/HDL-C ratio can be regarded as a significant risk factor for the development of gestational diabetes. Early detection of elevated TG/HDL-C may serve in early detection of GDM and help physicians in framing primary preventive strategies.

Gestational diabetes mellitus

TG/HDL-C ratio

Serum lipid profile

risk factors

With an internationally rising incidence, Gestational diabetes mellitus (GDM) is defined as a pregnancy-related metabolic disorder[1]. The estimated prevalence of GDM ranges from less than 1–28%[2]. Moreover, GDM not only increases the risk of maternal and fetal perinatal complications in the short term but also increases the risk of subsequently developing type 2 diabetes mellitus (T2DM) and cardiovascular disease in the long term [3–5]. Besides, the offspring of GDM mothers have increased risk of obesity, increased adiposity, disorders of glucose metabolism (insulin resistance and type 2 diabetes), and hypertension[6–9]. Obesity and abnormal lipid profiles are significant risk factors[10–11]. Therefore, intensified surveillance, early detection of risk factors, and active interventions may lower the rates of the adverse outcomes.

Increased TG/HDL-C has been regarded as one of the significant markers for Insulin resistance[12]. Several studies have reported signifcant associations of the TG/HDL-C ratio with metabolic syndrome [13]. This study aimed to explore the correlation between the ratio of triglycerides to high-density lipoprotein cholesterol (TG/HDL-C) in the blood and GDM in the first trimester, in order to provide a theoretical basis for the early identification and management of GDM, as well as prevent the development of GDM.

Study Population

Participants were selected from patients in Shanghai General Hospital Affiliated with Shanghai Jiaotong University. The inclusion criteria of subjects were: (a) selection period from January 2020 to June 2021, regular obstetric examinations and deliveries; (b) complete baseline data and relevant laboratory indicators during pregnancy; and (c) no long-term use of glucocorticoids, contraceptives, adrenal gland blockers, and other drugs that interfere with fasting blood glucose levels. Participants were excluded if they: (a) had a previous diagnosis of liver and kidney insufficiency, polycystic ovary syndrome (PCOS), and pancreatitis; (b) multiple pregnancy and assisted reproduction; (c) took lipid-lowering drugs; (d) type 1 or type 2 diabetes mellitus before or during pregnancy; (e) medical abortion or experienced intrauterine fetal death.

Ethical considerations

The study complies with the Helsinki Declaration. This study involving human participants were reviewed and approved by the Ethics Committee of the Shanghai General Hospital of School of Medicine, Shanghai Jiao Tong University. The patients/participants provided their written informed consent to participate in this study.

Data collection

The following maternal characteristics were assessed: age, pre-BMI, gravidity, and parity at first prenatal visit. Results of biochemistry tests were also collected including fasting plasma glucose (FPG), hemoglobin A1c (HbA1c), total cholesterol (TC), triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), low-density lipoproteins cholesterol (LDL-C), apolipoprotein A1 (ApoA1), apolipoprotein B (ApoB), apolipoprotein E (ApoE), and free fatty acid (FFA). All laboratory measurements were performed within 3 days after the first clinical visit using the Hitachi 7180 automatic biochemical analyzer. The samples were stored at 4℃ and were analyzed within 4 hours after collection. The obstetric outcomes assessed the rate of caesarean section (CS), GDM.

Diagnostic criteria

GDM screening was conducted in 24–28 weeks of gestation using oral glucose tolerance tests (OGTT). During the test, pregnant women were given 75 g of glucose after an overnight fasting, and blood glucose levels were measured before and at 1 and 2 h after oral administration. The GDM diagnostic criteria using recommendations from the International Association of Diabetes in Pregnancy were a fasting glucose concentration (0h-OGTT) ≥ 92 mg/dL (5.1 mmol/L), 1-hour glucose concentration (1h-OGTT) ≥ 180 mg/dL (10.0 mmol/L), and/or 2-hour glucose concentration (2h-OGTT) ≥ 153 mg/dL (8.5 mmol/L).

Statistical analysis

Data were expressed as the mean ± standard deviation for normally distributed variables and comparisons among subgroups were analyzed by a t test or one-way ANOVA. If the normality was rejected then nonparametric test was used. Logistic regression was performed to extensively identify the factors related to the incidence of GDM. Te odds ratio (OR) and 95% confdence interval (CI) were used to estimate the strength of the association. Additionally, associations between the TG/HDL ratio and the risk of GDM were evaluated on a continuous scale with restricted cubic spline (RCS) curves. The count of knots was determined by assessing the AIC of the univariate models. Probable linearity was identifed by utilizing a likelihood ratio test comparing the model with only a linear item and the model with linearly added cubic spline items [14]. Statistical analyses were completed in R 4.1.2 and IBM SPSS Statistics 27, Armonk, NY, USA.

Baseline characteristics of participants

The characteristics of the 2, 356 individuals included in this study are shown in Table 1. A total of 425 (18.04%) participants developed gestational diabetes mellitus. As shown in Table 1, patients with GDM had a higher rate of cesarean section, and had increased BMI, FPG, HbA1c, TC, TG, LDL-C, ApoA1, ApoB, ApoE, FFA, and TG/ HDL ratio than patients without non-GDM (all P < 0.05).

Table 1

Characteristics and lipid values in early pregnancy
Variables		GDM group (n = 425) M(P25,P75)/N(%)	Non-GDM group (n = 1931) M(P25,P75)/N(%)	P-value
Demographic characteristics
Mode of delivery	Caesarean delivery	284(66.8)	1046(54.2)	< 0.001***
	Vaginal delivery	141(33.2)	885(45.8)
Maternal age(years)	< 35	353(83.1)	1646(85.2)	0.099
	≥ 35	72(16.9)	285(14.8)
pre-BMI(kg/m2)	< 28	392(92.2)	1811(93.8)	< 0.001***
	≥ 28	33(7.8)	120(6.2)
Gravidity	1	121(28.5)	719(37.2)	0.015*
	2	143(33.6)	613(31.8)
	≥ 3	161(37.9)	599(31.0)
Parity	0	204(48.0)	1068(55.3)	0.065
	1	190(44.7)	737(38.2)
	≥ 2	31(7.3)	126(6.5)
Biochemical indicators
FPG(mmol/L)		5.09(4.73,5.42)	4.56(4.24,4.85)	0.000***
HbA1C(%)		5.20(4.90,5.50)	5.10(4.90,5.30)	< 0.001***
TC(mmol/L)		5.04(4.47,5.60)	4.79(4.27,5.36)	< 0.001***
TG(mmol/L)		1.55(1.22,1.97)	1.39(1.09,1.79)	< 0.001***
HDL-C(g/L)		1.65(1.38,1.89)	1.60(1.37,1.85)	0.117
LDL-C(g/L)		2.47(2.07,2.95)	2.39(2.00,2.86)	0.012
ApoA1(g/L)		1.71(1.54,1.87)	1.65(1.49,1.80)	< 0.001***
ApoB(g/L)		0.72(0.62,0.86)	0.69(0.59,0.81)	< 0.001***
ApoE(g/L)		28.00(19.00,41.00)	37.00(29.00,47.00)	< 0.001***
FFA(mmol/L)		0.65(0.46,0.82)	0.60(0.45,0.74)	0.007**
TG/HDL-C		0.95(0.71,1.28)	0.87(0.64,1.18)	< 0.001***
P < 0.05;P < 0.01༛**P < 0.001

Risk factors for GDM

Univariate Logisitic regression analysis showed that FPG, HbA1c, TC, TG, ApoA1, ApoE, FFA, and TG/ HDL-C ratio were signifcantly associated with GDM (all P < 0.05). Stepwise multivariate Logisitic regression analysis indicated that individuals whose TG/HDL-C ratio was high were more likely to develop GDM (OR: 1.61, 95% CI: 1.26– 2.05). Compared with the non-GDM, subjects had higher rate of cesarean section, with corresponding OR (95% CI) of 1.70 (1.33–2.18). Furthermore, participants with higher FPG (OR: 6.13, 95% CI: 4.65–8.09), HbA1c (OR: 1.68, 95% CI: 1.21–2.32), TC (OR: 1.19, 95% CI: 1.01–1.41), ApoA1 (OR: 2.64, 95% CI: 1.49–4.69) and ApoE (OR: 0.98, 95% CI: 0.97–0.99) were more likely to develop GDM.

Table 2

Risk analysis of GDM
Variables	Univariate analysis			Multivariate analysis
	P	OR	95%CI	P	OR	95%CI
Biochemical indicators
FPG(mmol/L)	< 0.001***	9.08	(7.01,11.77)	< 0.001***	6.12	(4.64,8.08)
HbA1C(%)	< 0.001***	3.28	(2.46,4.39)	0.002**	1.68	(1.21,2.32)
TC(mmol/L)	< 0.001***	1.31	(1.16,1.47)	0.035*	1.19	(1.01,1.41)
TG(mmol/L)	< 0.001***	1.46	(1.26,1.69)
HDL-C(g/L)	0.078	1.20	(0.98.1.46)
LDL-C(g/L)	0.061	1.15	(0.99,1.32)
ApoA1(g/L)	< 0.001***	2.83	(1.84,4.35)	< 0.001***	2.64	(1.49,4.69)
ApoB(g/L)	0.283	1.14	(0.90,1.44)
ApoE(g/L)	< 0.001***	0.98	(0.97,0.98)	< 0.001***	0.98	(0.97,0.99)
FFA(mmol/L)	0.005**	1.88	(1.21,2.94)
TG/HDL-C	< 0.001***	1.37	(1.16,1.62)	< 0.001***	1.61	(1.25,2.03)
P < 0.05;P < 0.01༛**P < 0.001

TG/HDLC ratio and risk of GDM

The relationship of the TG/HDL-C ratio with the occurrence of GDM is summarized in Table 3. Model 1 shows the association between the TG/HDL- C ratio and GDM without adjusting for any confounders. It is obvious that the TG/HDL-C ratio is an independent risk factor for GDM, with corresponding OR (95% CI) of 1.37 (1.16–1.62). The TG/HDL-C ratio increased by 1 mmol/L, and the risk of GDM was augmented by 27% in the adjusted model (model 2). Additionally, after adjusting for all potential confounders, we found

that the TG/HDL-C ratio is still an independent risk factor for GDM (OR = 1.65 (95% CI: 1.27–2.13), p < 0.001).

Table 3

Logistic regression results of the association of patient characteristics with GDM
Model	Exposure	B	P value	OR (95% CI)
Model 1	TG/HDL-C	0.32	< 0.001***	1.37(1.16,1.62)
Model 2	TG/HDL-C	0.24	0.006**	1.27(1.07,1.50)
	pre-BMI	0.06	< 0.001***	1.06(1.03,1.09)
Model 3	TG/HDL-C	0.50	< 0.001***	1.65(1.27,2.13)
	pre-BMI	0.05	0.004**	1.06(1.02,1.09)
	FPG	1.82	< 0.001***	6.15(4.66,8.11)
	HbA1C	0.48	0.005**	1.61(1.16,2.25)
	HDL-C	0.31	0.023*	1.36(1.04,1.78)
	ApoA1	0.98	< 0.001***	2.66(1.51,4.70)
	ApoE	-0.03	< 0.001***	0.98(0.97,0.98)
P < 0.05;P < 0.01༛**P < 0.001
Model 1: crude model; Model 2: adjusted for Maternal age, BMI, Gravidity, Parity; Model 3: adjusted for any confounders.

Supplementary analysis

The occurrence rates of gestational diabetes were 20.2% when the TG/HDL-C ratio was > = 0.75, 21.3% when the TG/HDL-C ratio was > = 1.00, 21.8% when the TG/HDL ratio was > = 1.25, and 25.6% when the TG/HDL-C ratio was > = 1.5, respectively. These rates were significantly higher compared to the incidence of gestational diabetes when the TG/HDL-C ratio was < 0.75 (14.1%), < 1.00 (16.1%), < 1.25 (17.0%), and < 1.5 (16.9%)(Figs. 1–4). We plotted the RCS to explore the nonlinear correlation between the TG/HDL-C ratio, as shown in Fig. 5 (P for nonlinearity < 0.05 in adjusted Model 3).

In this study, we observed close associations between TG/HDL-C and GDM in the first trimester. This study proved that the TG/HDL-C ratio was an independent risk factor for GDM, and RCS analysis showed a nonlinear relationship between the TG/HDL-C ratio and GDM.

TG and HDL-C are part of the diagnostic criteria in MetS, but the International Diabetes Association does not include TG/HDL-C ratio in the diagnosis of MetS[15]. The metabolic syndrome (MetS) is a group of cardiovascular risk factors that are associated with insulin resistance and are driven by underlying factors, including visceral obesity, systemic inflammation, and cellular dysfunction[16]. However, TG/HDL-C ratio seems to play an important role in metabolic disorders[17]. Hirschler et al.’s results, whose study on the application of the TG/HDL-C ratio to predict insulin resistance analysed IR in children of different age groups, showing a higher degree of IR in children of older age[18]. A huge number of studies have shown that TG/ HDL-C can be used as a significant indicator of insulin resistance[19–20]. A study showed that the TG/HDL-C ratio had high sensitivity (80%) and specificity (75%) to MetS, with a cut- off point of 1.25[17]. Studies on the association between TG/HDL and MetS were rare. Besides, A huge number of clinical trials to date have proved that lipid metabolism disorder has toxic effects on cells, which can affect the function of islet β cells and cause or aggravate insulin resistance. Insulin resistance and deficiency of insulin secretion can further aggravate lipid metabolism disorders[21–22]. Additionally, GDM is characterized by insulin resistance and insulin insufficiency during pregnancy. As pregnancy progresses, the placenta gradually increases the secretion of anti-insulin hormones (prolactin, progesterone, estradiol and placental growth hormone), which results in an increased insulin demand from pancreatic β cells[23–24]. Therefore, it is inevitable to explore the association between TG/HDL-C and GDM.

In our study, We found that TG/HDL-C was significantly positive correlated with GDM. Logistic regression analysis showed that the TG/HDL-C ratio was an independent risk factor for GDM (OR = 1.37 (95% CI: 1.16–1.62), p < 0.001). In order to eliminate these variables known to be associated with GDM, we performed a logistic regression analysis to eliminate the interference of these confounding factors, we observed that a high TG/HDL-C ratio promoted GDM(OR: 1.65, 95% CI: 1.27–2.13, p < 0.001). The RCS analysis revealed a signifcant nonlinear association(P-interaction < 0.05). Therefore, we need to attach great importance to the women’s lipid profiles. The early detection of pregnant women at a high risk for GDM through the measurement of the TG/HDL-C ratio can help to actively prevent or treat them before disease symptoms appear, thus providing women with the greatest clinical benefit.

Among the main strength of this study is that it provides new evidence for the potential association between TG/HDL-C ratio and GDM. The present study also assesses a wide range of confounding factors. Finally, the large sample size design should also be noticed when interpreting the results. Risk thresholds for the TG/HDL-C ratio should be established in large cohorts, identifying those at high risk for GDM prevention.

Several limitations should also be recognized in the current study. First, there are inherent limitations such as missing data and selection bias in the study. Second, the study lacks detailed information on vegetable, cereal, high-fat and high-fber diet intake, which prevents us from examining confounding variables precisely. In addition, this population-based study did not deeply explore the mechanisms for the associations between first-trimester TG/HDL-C ratio and the risk of GDM in early pregnancy. Multi-center prospective studies can be conducted to expand the sample size to further verify the value of TG/HDL-C ratio for GDM screening in early pregnancy. In addition to know the effects of dietary factors on TG/HDL-C, it is necessary to conduct animal or cell experiments in the further study and explore the underlying mechanism of TG/HDL-C in the ocurrence and development of GDM.

We showed a strong association between TG/HDL-C ratio and the occurrence of GDM. Subjects with dyslipidemia should be the critical intervention population. Women are likely to beneft from lipidlowering interventions and thus avoid GDM. This study is of vital importance for the early identification and management of GDM. The measurement of the TG/HDL-C ratio can help clinicians to identify pregnant women who need targeted treatment, management and follow- up.

BMI Body mass index

DM Diabetes mellitus

GDM Gestational diabetes mellitus

OGTT Oral Glucose Tolerance Test

SD Standard deviation

TG/HDL-C ratio triglyceride/high-density lipoprotein cholesterol ratio

RCS restricted cubic spline

Acknowledgments

The authors thank all the participants in this study.

Funding

Project name: To promote clinical skills and clinical innovation ability of municipal hospitals: three-year action plan project. Project number: SHDC2020CR2060B. Setting: Shanghai Shenkang Hospital Development Center.

Contributors

X.X. contributed to the concept and design of the study. H.J. , L.C, P.H., S.Z. and M.Z. contributed to data collection. H.J. wrote the manuscript. C.L reviewed and edited the manuscript. H.J. and M.Z. is the guarantor of this work and, as such, has full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. We thanked all patient advisers involved in this study.

Competing interests

We declare no conflict of interest.

Patient and public involvement

Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research. Patient consent for publication Consent obtained from patients.

Ethics approval statement

This study involving human participants were reviewed and approved by the Ethics Committee of the Shanghai General Hospital of School of Medicine, Shanghai Jiao Tong University. The patients/participants provided their written informed consent to participate in this study.

Provenance and peer review

Not commissioned; externally peer reviewed.

Data availability statement

Data are available upon reasonable request. The datasets generated during and/or analysed during the current study are available upon reasonable request through the corresponding author.

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No competing interests reported.

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You are reading this latest preprint version

High TG/HDL-C ratio suggests a higher risk of gestational diabetes mellitus in the first trimester

Status:

Version 1

Abstract

Figures

Background

Methods

Study Population

Ethical considerations

Data collection

Diagnostic criteria

Statistical analysis

Results

Baseline characteristics of participants

Risk factors for GDM

TG/HDLC ratio and risk of GDM

Supplementary analysis

Discussion

Conclusions

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1