Gamma-glutamyl transferase to high-density lipoprotein cholesterol ratio and endometriosis: a population-based study

Background The gamma-glutamyl transferase (GGT) to high-density lipoprotein (HDL) ratio (GGT/HDL) has recently emerged as a potential biomarker for metabolic and liver diseases. This study aimed to investigate the association between GGT/HDL ratio and endometriosis using a population-based dataset from the National Health and Nutrition Examination Survey (NHANES).

Data from NHANES 1999 to 2006 were used to assess the relationship between the GGT/HDL ratio and endometriosis. The diagnosis of endometriosis was based on self-reported data from the Reproductive Health Questionnaire. The GGT/HDL ratio was calculated and Ln-transformed for analysis. Multivariable logistic regression and sensitivity analysis were used to estimate the odds ratio (OR) for endometriosis in relation to the GGT/HDL ratio.

A total of 3815 individuals were included, with 307 diagnosed with endometriosis. The Ln-transformed GGT/HDL ratio was positively associated with the endometriosis. Each unit increase in the Ln-GGT/HDL ratio was associated with a 22% higher likelihood of endometriosis (OR = 1.220, 95% CI: 1.003–1.483, p = 0.046). Sensitivity analyses including the use of original GGT/HDL value, the further adjustments of covariates, the exclusion of those with CVD and liver diseases confirmed the robustness of this association.

This study found a significant positive association between the GGT/HDL ratio and endometriosis. Higher GGT/HDL levels may serve as a potential biomarker for identifying women at risk of endometriosis. Plain Language Summary This study investigated the relationship between the gamma-glutamyl transferase (GGT) to high-density lipoprotein (HDL) ratio (GGT/HDL) and endometriosis, using data from the National Health and Nutrition Examination Survey (NHANES) from 1999 to 2006. GGT/HDL were from laboratory tests and endometriosis diagnosis was based on self-reported information from the Reproductive Health Questionnaire. The study included 3815 individuals, of whom 307 were diagnosed with endometriosis. The results showed that a higher GGT/HDL ratio was associated with a higher risk of endometriosis. Specifically, for each unit increase in the Ln-GGT/HDL ratio, the likelihood of having endometriosis increased by 22%. This association remained robust even after conducting sensitivity analyses. The findings suggested that the GGT/HDL ratio could be a useful biomarker for identifying women at risk of developing endometriosis.

Endometriosis is a chronic, inflammatory, gynaecologic systemic disease characterised by the abnormal presence of endometrial-like tissue outside the uterus, primarily manifesting as pain and fatigue, with an increased risk of infertility (Horne and Missmer Citation2022). Affecting approximately 5–10% of women of reproductive age globally, endometriosis is now considered a systemic disease characterised by systemic inflammation resulting from the unbalanced metabolism of liver and adipose tissues (Taylor et al. Citation2021). Growing evidence links endometriosis to atherosclerosis, cardiovascular disease (CVD) and pre-eclampsia (Tulandi and Vercellini Citation2024). Furthermore, endometriosis may be associated with autoimmune diseases and cancer (Shigesi et al. Citation2019, Kvaskoff et al. Citation2021). As an inflammatory systemic disease, its diagnosis may involve more than just the disease itself, considering its multi-organ effects. As a challenging condition, endometriosis imposes high individual and societal costs, and the gold standard for diagnosis is surgery, which may impact surgical morbidity and ovarian reserve (Falcone and Flyckt Citation2018). Previous studies have shown that fibrosis may exacerbate endometriosis-associated pain, sharing similar pathology with liver cirrhosis (Vissers et al. Citation2024). Endometriosis leads to decreased body weight and fat, and disrupts liver gene expression, suggesting that liver-mediated metabolism may be a characteristic feature of women with endometriosis (Goetz et al. Citation2016). These findings suggest that liver function may be connected to endometriosis. Gamma-glutamyl transferase (GGT) is associated with metabolic syndrome (MetS), hepatic steatosis and advanced fibrosis in patients with non-alcoholic fatty liver disease (NAFLD) (Chen et al. Citation2021), and is widely used to evaluate liver dysfunction and alcohol intake (Whitfield Citation2001). Furthermore, high-density lipoprotein (HDL), primarily synthesised and metabolised by the liver, is associated with liver function and prognosis in liver diseases (Habib et al. Citation2005). Notably, endometriosis can also occur in the liver (hepatic endometriosis), presenting diagnostic challenges perioperatively, with surgical resection yielding favourable outcomes (Prodromidou et al. Citation2020). Similarly, laparoscopy-diagnosed endometriosis is associated with the risk of NAFLD incidence, as shown in the Nurses’ Health Study (Huang et al. Citation2025). Alanine transaminase (ALT), a liver biomarker, is correlated with the severity of endometriosis (Zhong et al. Citation2025). Meanwhile, individuals with endometriosis have higher levels of non-HDL and low-density lipoprotein (LDL) (Melo et al. Citation2010). Additionally, genetically predicted triglycerides (TRs), HDL, LDL and apolipoprotein A are associated with endometriosis (Zhou et al. Citation2024). The literature suggests that liver biomarkers may be used in the diagnosis and surveillance of endometriosis. The GGT/HDL ratio has been recently proposed as an indicator of metabolic associated fatty liver disease (MAFLD) and MetS in individuals with type 2 diabetes (T2DM) in China, and NAFLD, severity of hepatic steatosis, and liver fibrosis in U.S. (Xing et al. Citation2022, Gong et al. Citation2023, Wang et al. Citation2025). Furthermore, the GGT/HDL ratio could also serve as a predictor of T2DM prevalence, with a higher ratio indicating an increased risk of T2DM (Xie et al. Citation2022). Additionally, the GGT/HDL ratio was correlated with cognitive score measured by the digit symbol substitution test (DSST) (Wang et al. Citation2025). Given the diagnostic delays and misdiagnoses of endometriosis, the development and use of simple, non-invasive serum and lipid biomarkers for endometriosis identification and prompt treatment is crucial. Using a nationally representative sample from the U.S. based on the National Health and Nutrition Examination Survey (NHANES) from 1999 to 2006, this study aims to explore the association between the GGT/HDL ratio and the prevalence of endometriosis, providing new insights into the role of liver function and lipid traits in the risk of endometriosis. The hypothesis is that the GGT/HDL ratio is positively associated with the prevalence of endometriosis.

Study design NHANES is a biennial, comprehensive survey conducted in the United States by the National Center for Health Statistics (NCHS), part of the Centers for Disease Control and Prevention (CDC), to assess the health and nutritional status of non-institutionalised U.S. individuals. The NHANES protocol was revised and approved by the Ethics Review Committee of NCHS, ensuring that all participants provided written informed consent, with the protocol NCHS ERB Protocol Number: Protocol #98-12 and Protocol #2005-06. All the data can be accessed directly on an online website (https://www.cdc.gov/nchs/nhanes/). This study is based on NHANES data from 1999 to 2006, which includes four cycles. The calculation of GGT/HDL The GGT/HDL ratio was calculated as GGT (U/L)/HDL (mmol/L). GGT and HDL were derived from laboratory tests. In the analyses, the GGT/HDL ratio was Ln-transformed (Ln-GGT/HDL) to address its skewness and then categorised into quartiles. The determination of endometriosis The diagnosis of endometriosis was based on a self-reported questionnaire coded RHQ360 in the Reproductive Health Questionnaire that was only available in year from 1999 to 2006, specifically asking, ‘Has a doctor or other health professional ever told you that you had endometriosis?’ An affirmative answer to this question was used to determine the presence of endometriosis. This definition has been reported in previous studies in NHANES based investigation (Chen et al. Citation2025, Jiang et al. Citation2025). Although it lacks the gold standard for diagnosing endometriosis, self-reported endometriosis is reasonable, with high accuracy, and is thus utilised in this study (Shafrir et al. Citation2021). Covariates In line with previous studies, several confounders were included (Zhao et al. Citation2024, Zheng et al. Citation2025b). This study included various demographic factors, chronic diseases and reproductive health-related covariates. Demographic factors included age, race, education level, marital status and poverty level as measured by the poverty income ratio (PIR). Smoking status and alcohol consumption were also included. Additionally, chronic diseases included diabetes mellitus, hypertension, CVD and liver conditions, with obesity status measured by body mass index (BMI) also included. Reproductive health covariates included the use of oral contraceptives and exogenous female hormone preparations. Details of the covariates’ definitions are presented in Table S1. Statistical analyses The baseline characteristics of the included participants were categorised into two groups based on the presence or absence of endometriosis. Continuous variables were expressed as mean ± standard deviation (SD), while categorical variables were expressed as frequency (n) and proportions (%). Weighted Student’s t-tests and weighted Chi-square tests were used to compare continuous and categorical baseline characteristics, respectively. The continuous and quartile-based Ln-GGT/HDL ratios (≤2.076, 2.076–2.465, 2.465–2.961, ≥2.961), using the lowest quartile as the reference, were analysed as exposures. A recalculated combined proportional weight was applied, using 4/8 of WTMEC4YR (NHANES 1999–2002) and 2/8 of WTMEC2YR (2003–2006), to mitigate unequal selection and nonresponse bias, and this study used SDMVSTRA/SDMVPSU in the survey setting. Univariate and multivariate weighted logistic regression models were then used to assess the relationship between GGT/HDL and endometriosis, and the corresponding odds ratio (OR) and confidence interval (CI) were calculated. Three models were established: model I (no adjustment), model II (adjustments for age, race, poverty, marital status and education level) and model III (adjustments for age, race, poverty, marital status, education level, BMI, smoking, alcohol consumption, diabetes, hypertension and CVD). To explore the association between GGT/HDL and endometriosis, subgroup analyses were conducted based on age, race, poverty level, obesity status, smoking and alcohol status, diabetes, hypertension and CVD, and interactions were also investigated. Sensitivity analyses were conducted, including associations between the original GGT/HDL value and endometriosis, further adjustments for birth control pills, hormone use and liver conditions, as well as excluding individuals with CVD and liver conditions, and 2.5% proportion of bottom and top Ln-GGT/HDL value. A non-linear relationship was detected using restricted cubic spline (RCS) analysis with three knots at the 25%, 50% and 75% percentiles of the data. All analyses accounted for the survey weight using R software (version 4.3.3) (The R Project for Statistical Computing, Vienna, Austria). A p value less than 0.05 was considered statistically significant.

The baseline characteristics of the included population illustrates the screening process based on inclusion and exclusion criteria for participants. A total of 3815 individuals were included in this study, with 307 subjects diagnosed with endometriosis and 3508 without, resulting in a weighted prevalence of 9.80% in the population, the age of the included participants ranged from 20 to 54, with a median age of 38. The baseline characteristics of participants are detailed in , categorised by endometriosis status. Individuals with endometriosis tended to be older, of non-Hispanic White ethnicity, highly educated, married and current smokers. They were also more likely to be non-diabetic, non-hypertensive, and have a history of oral contraceptive and non-female hormone use. There was no difference in GGT, HDL and GGT/HDL between the two groups; however, the Ln-GGT/HDL values for individuals with and without endometriosis were 2.60 and 2.50, respectively, showing a statistically significant difference. Association between GGT/HDL and endometriosis As shown in , there was a positive correlation between Ln-GGT/HDL and the risk of endometriosis. Models I, II and III maintained the same direction when Ln-GGT/HDL was treated as a continuous variable. Each unit increase in Ln-GGT/HDL was associated with a 22% increased likelihood of endometriosis (OR = 1.220; CI, 1.003–1.483, p = 0.046) in the fully adjusted model. When Ln-GGT/HDL was treated as a quartile variable, participants in the highest quartile had a 52% increased risk of endometriosis (OR = 1.521; CI, 1.019–2.271, p = 0.041) after full adjustment for covariates, compared to those in the lowest quartile. Trend analysis also revealed a significant association, suggesting that higher Ln-GGT/HDL levels are associated with an increased risk of endometriosis (p for trend < 0.05). In the sensitivity analyses, when the original value of GGT/HDL was used as exposure (shown in ), similar results were found in model III (OR = 1.004; CI, 1.001–1.007, p = 0.017). Additionally, after further adjustments of oral contraceptive, hormones use and liver condition (Table S2), each unit increase in Ln-GGT/HDL and the fourth quartile were associated with a 23% and 54% increase of endometriosis. Lastly, after excluding those with CVD and liver condition, and 2.5% proportion of bottom and top Ln-GGT/HDL value, similar results were also detected (Tables S3 and S4). Those sensitivity analyses provided robustness of the relationship between GGT/HDL and the risk of endometriosis. Subgroup and RCS analysis Stratified analyses () were conducted in different factors including age, education, poverty, BMI, smoke, alcohol use, diabetes, hypertension and CVD; results revealed that the correlation between Ln-GGT/HDL and endometriosis were stable in all subgroups and no interaction was found. RCS analysis () suggested the presence of a linear relationship, with higher levels of Ln-GGT/HDL were correlated with increased risk of endometriosis (p for nonlinear = 0.3161). RCS analysis of the primitive value of GGT/HDL (Figure S1) also identified similar results with a linear relationship. These analyses enhanced the evidence that GGT/HDL was positively associated with endometriosis.

In the present study, the association between GGT/HDL ratio and the risk of endometriosis was unveiled. The findings indicated that higher levels of GGT/HDL ratio were associated with an increased risk of endometriosis based on a large and representative sample of U.S. women. This relationship remained robust even after adjusting for potential confounders and sensitivity analyses. This biomarker could be used in clinical practice in the management of reproductive health. The findings of this study are consistent with previous research. In a prospective study, the GGT/HDL ratio was correlated with an increased incidence of CVD in women in Korea (Jung et al. Citation2023). Lower GGT/HDL ratio was also associated with the resolution of MetS within 6 months after bariatric surgery in individuals with MetS (Lizarbe-Lezama et al. Citation2024). These conditions share similar risk factors with endometriosis. Endometriosis has been reported to be associated with malignant tumours, migraines, pelvic inflammatory disease (PID), infertility, obesity, chronic liver disease, arthritis, diabetes, and an increased risk of CVD and hypertension (Teng et al. Citation2016, Okoli et al. Citation2023, Parsa et al. Citation2025). Regarding the association between liver disease and endometriosis, individuals with endometriosis had a higher proportion of PID, CVD, chronic liver disease and rheumatic disease in Taiwan, China (Wang et al. Citation2014). Based on the Nurses’ Health Study II, laparoscopically confirmed endometriosis was positively associated with NAFLD, and hysterectomy, hypercholesterolaemia, hypertension and infertility mediated this relationship (Huang et al. Citation2025). In postmenopausal women, MAFLD was positively associated with endometrial thickness, as was increased BMI (Wei et al. Citation2021). In the relationship between endometrial cancer (EC) and liver disease, NAFLD was associated with an increased risk of early-onset EC, and young individuals with NAFLD and obesity had a synergistic effect (Park et al. Citation2025). Elevated hepatic steatosis index was an independent risk factor for EC, and GGT and HDL were significantly correlated with EC occurrence (Zheng et al. Citation2025a). In addition, fibrosis-4 (FIB-4) score and GGT were biochemical markers for type 1 EC (Rakici et al. Citation2025). The aforementioned evidence suggests that endometriosis may facilitate the incidence and progression of liver disease; however, direct evidence of liver disease influencing the risk of endometriosis is limited and warrants further studies. Then, alterations in lipid metabolism were also observed. Individuals with endometriosis had a higher risk of low HDL, increased waist circumference, and MetS (Saei Ghare Naz et al. Citation2024). Similar findings were reported, showing that endometriosis patients had increased LDL and non-HDL cholesterol levels (Melo et al. Citation2010). However, in a meta-analysis, only elevated TGs were identified as a risk factor for endometriosis, while the others were not (Yang et al. Citation2025). Lipid-based or synergistic biomarkers have shown their effectiveness. TG was associated with an increased risk of endometriosis, while HDL may serve a protective role in both NHANES and Mendelian randomisation studies (Peng et al. Citation2024). The non-HDL/HDL cholesterol ratio (NHHR) was correlated with endometriosis development (Jiang et al. Citation2025). Additionally, higher remnant cholesterol (RC) and atherogenic index of plasma (AIP) were associated with an elevated prevalence of endometriosis (Chen et al. Citation2025, Liu et al. Citation2025). In Japanese women, elevated hypertriglyceridaemia was a risk factor for elevated GGT levels and fatty liver, suggesting that MetS is directly associated with raised GGT levels (Sakugawa et al. Citation2004). The underlying mechanisms of the relationship of GGT/HDL ratio and the risk of endometriosis are unclear, but could be attributed to systemic inflammation and alterations of gut microbiome. In those with endometriosis, increased PI3K/AKT signalling pathway, pyroptosis and inflammation were observed with higher levels of IL-1β, and IL-18 (An et al. Citation2024). In the peritoneal fluid of women in advanced-staged endometriosis, the levels of oxidised LDL were increased, suggesting oxidative stress may play a role (Polak et al. Citation2011). Mediterranean diet (MD) benefitted to the metabolic, oxidative profile, as well as overall health quality of life measured by rapid movement of physical activity in those patients with endometriosis (Cirillo et al. Citation2023). The two liver enzymes, ALT and GGT, had been regarded as marker of systemic inflammation and oxidative stress, which was independent of MetS (Yamada et al. Citation2006). Then, HDL, its versatility may be utilised in an-inflammation therapy, and minor alterations in systemic inflammation may bring the dysfunction of HDL endothelial protective effect (Säemann et al. Citation2010, O’Neill et al. Citation2015). Then, study revealed that the intestinal permeability was abnormal with high levels of serum LPS, which may be a pathogenesis of this chronic disease (Viganó et al. Citation2020). Endometriosis may induce gut microbiome dysbiosis, and gut microbiome and flora-derived metabolites may also contribute to the lesion of endometriosis (Yuan et al. Citation2018, Chadchan et al. Citation2023). In those MetS men with elevated GGT, the microbial composition differed, with increasing levels of harmful bacteria (Sheng et al. Citation2022). Gut microbiome also shaped the lipoproteins distribution (LPD), those with healthy LPD exhibited high abundance of B-vitamins and faecal short-chain fatty acids (Castro-Mejía et al. Citation2022), and explained the 25.9% variability of BMI, TG and HDL independent age, sex and host genetics (Fu et al. Citation2015). However, the extent to which the GGT/HDL ratio influences systemic inflammation and gut microbiome composition, either independently or synergistically, requires further investigation. The relationship between metabolic risk factors, liver biomarkers, lipid metabolism and endometriosis remains unclear due to differences in populations and the severity of endometriosis. However, it should be acknowledged that there are limitations in this study. First, its design precluded establishing causality between GGT/HDL changes and endometriosis due to its cross-sectional nature. Second, the diagnosis of endometriosis was based on self-reported questionnaires rather than surgical confirmation, which may introduce potential recall biases and misclassification. Third, subgroup analyses were not corrected for multiple comparisons, which may lead to type I error. Fourth, the OR in this study was borderline, and the interpretation should be cautious. Lastly, this study was based in the U.S., and further studies in diverse populations and regions are needed to validate the results.

This study is the first to suggest a positive association between the GGT/HDL ratio and endometriosis. Elevated GGT/HDL levels may be of clinical interest in individuals diagnosed with or at risk for endometriosis. These findings highlight the potential value of this biomarker in supporting diagnosis, prevention and prognostic assessment; although, further validation is needed to establish any causal relationship. Ethical approval The studies involving human participants were approved by the Ethics Review Board of the National Center for Health Statistics. They were conducted in accordance with local regulations and institutional guidelines. Consent form All participants provided their written informed consent. Supplemental material cleaned Supplementary_material.docx Download MS Word (1 MB)cleaned Supplementary_material.docxAcknowledgements The authors appreciate the NHANES open policy and the provided data as well as all participants and staffs in this study. Disclosure statement No potential conflict of interest was reported by the author(s). Data availability statement The findings of this study are supported by data from the NHANES (National Health and Nutrition Examination Survey). The dataset is publicly available and can be accessed directly at the following link: https://www.cdc.gov/nchs/nhanes/. Additional information Funding

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