To the best of our knowledge, this study is the first study to compare the discriminatory potentials of fatty liver index (FLI) and triglyceride glucose index (TyG) for detecting hepatic steatosis in Chinese nondiabetic postmenopausal women. In this study, we found that both FLI and TyG had the significantly higher odds ratio for hepatic steatosis than their respective reference after adjusting for the potential confounders. Moreover, we also found that FLI is a superior surrogate index than TyG for detecting the presence of hepatic steatosis in Chinese nondiabtic postmenopausal women. Furthermore, when TyG was added to each obesity index, the superiority of FLI over each combination is still significant. In conjunction with our previous findings [31], where we have identified that FLI is a better marker for predicting the presence of hepatic steatosis in postmenopausal women compared with several obesity indices including BMI, WC, WHR, WHtR, and visceral adiposity index, it seems that FLI may be the first choice when screening for hepatic steatosis in Chinese nondiabetic postmenopausal women.
Globally, the prevalence of NAFLD is estimated to be about 25% and often accompanies an increased prevalence of overweight or obesity [44]. With the introduction of westernized lifestyle and increasing frequency of obesity in the Asia-Pacific region including China, the prevalence of NAFLD has increased rapidly over the past two decades [7, 45, 46]. In this study, the prevalence of NAFLD was 29.3%, which is slightly higher than the result of a recent meta-analysis where the overall prevalence of NAFLD in Chinese adults was reported to be 20.1%. The explanation might be due to the different study population. However, the prevalence in this study is slightly lower than the result of one of our previous studies in which the prevalence of hepatic steatosis was 33.4% [31]. That is because we have excluded women with a history of T2DM or who were highly suspected of diabetes based on the results of physical examination, since NAFLD is closely associated with diabetes.
For women after menopause, fat distribution shifts from gluteofemoral subcutaneous adipose tissue (SAT) to abdominal visceral adipose tissue (VAT) [47]. It has been reported that significant increases in VAT only occur in those women who become postmenopausal during a four-year follow-up [48]. As a result, it is that the decrease of SAT as well as the increase of VAT makes postmenopausal women more prone to cardiometabolic disorders as compared with premenopausal women. Wong et al. reported that the prevalence of NAFLD was about two times higher in men compared with in women, but the prevalence of NAFLD in women increased with age and, in those older than 50 years, the prevalence of NAFLD became similar and even higher than that in men [49]. Considering that the average age of menopause is approximately 50 years, the assumption that menopause itself might affect metabolic changes and increase the development of NAFLD can be supposed [24].
It has been confirmed that there are close links between fatty liver and underlying insulin resistance, metabolic syndrome, T2DM, cardiovascular damage as well as cardiovascular events. Moreover, the clinical importance of NAFLD stems not only from its increasing prevalence in the general population but also its potential to progress to cirrhosis and liver failure [50]. A very recent review has demonstrated that individuals with evidence of NASH and advanced fibrosis are at markedly increased risk of adverse outcomes including overall mortality, and liver-specific morbidity and mortality, respectively [14]. Therefore, NAFLD has been becoming an increasingly recognized public health problem. In order to facilitate the screening of NAFLD in the population, a number of studies have been conducted with attempt to explore not only simple but also accurate markers. It has been confirmed that central obesity is definitely associated with NAFLD. In individuals with central obesity, an increased VAT results in an excessive production of inflammatory adipokines and hormones in conjunction with an increased lipolysis and influx of free fatty acid to the liver, which eventually leads to the synthesis of hepatic TG [51]. Therefore, obesity indices are frequently used in the screening of NAFLD [22–24]. According to Yoo et al., WC and WHtR were found to be as useful as dual-energy X-ray absorptiometry (DXA) and computed tomography (CT) for predicting NAFLD in adults aged 20–88 years [22]. Recently, Hong et al. have reported that WHR is a more accurate indicator for NAFLD than BMI and WC in postmenopausal women [24]. The possible explanation may be that WHR reflects the assumption ratio of abdominal VAT to gluteofemoral SAT, and it has been reported that the ratio of VAT to SAT is independently associated with the clustering of multiple cardiometabolic risk factors in women but not in men [52]. Further, because the hormone changes after menopause causes the deposition of abdominal VAT from the femoral SAT, the clinical significance of WHR might be more distinct after menopause [48]. Also, one of our previous studies showed that, among the indicators of central obesity, WHR is the best predictive marker for MetS development in Chinese postmenopausal women [40].
In addition to obesity indicators, the associations of other markers with NAFLD have been also investigated. Previously, we reported a index termed fatty liver index (FLI), which is an index firstly reported by Bedogni et al. and its score ranges from 0 to 100 [28]. A FLI of < 30 could be used to rule out (sensitivity = 87%) and a FLI of ≥ 60 to rule in hepatic steatosis (specificity = 86%) in an Italian population, thus, Bedogni et al suggested that the FLI was a simple and accurate predictor of hepatic steatosis. The validation of FLI in general populations has been confirmed in several studies [29, 30], and our previous study also showed that NAFLD assessed by FLI is well-correlated with hepatic steatosis using abdominal ultrasonography in Chinese postmenopausal women [31]. Unfortunately, there are few similar reports on the use of FLI to screen NAFLD in postmenopausal women other than our report, in which we compared the FLI and several frequently used obesity indices and found that FLI is generally better than indices including BMI, WC, WHR, WHtR, as well as visceral adiposity index in detecting hepatic steatosis in postmenopausal women.
NAFLD is considered as the liver manifestation of MetS and the two key components of MetS, triglyceride (TG) and fasting plasma glucose (FPG) are overproduced by the fatty liver [53]. Recently, the triglyceride glucose index (TyG) has been recommended as a reliable and simple surrogate marker for insulin resistance [33, 34, 54]. The close association between the TyG and liver steatosis has been demonstrated in people from Mexico and China [32, 55]. The explanation may be that TyG is a specific indicator of hepatic insulin resistance since it is well correlated with the amount of hepatic fat [32], whose amount predicts mortality and development of T2DM in individuals with NAFLD [56]. In addition, several studies have found that triglyceride to high-density lipoprotein cholesterol ration is independently associated with NAFLD as well as the severity of NAFLD [25, 26]. However, there are sparse studies specifically examining the association between TyG and hepatic steatosis among postmenopausal women.
In our present study, we firstly reported the comparison of the potential between FLI and TyG to detect hepatic steatosis in a population of menopausal women, and found that FLI is superior to TyG among postmenopausal women. After grouping by age, the superiority of FLI over TyG is unchanged. Unlike FLI, the TyG index does not contain variables that directly reflect body weight or body shape, although both FLI and TyG contain TG within them. Therefore, we further added obesity indices including BMI, WHR, or WHtR to the TyG to observe their combined effects to detect hepatic steatosis. Although the combined AUC of TyG plus each obesity index was slightly higher than that of TyG alone, the AUC value of FLI was still significantly larger than that of each combination, suggesting that FLI is a superior indicator for screening hepatic steatosis among postmenopausal women in a population-based study.
Strengths and limitations
This study firstly compares the differences in the ability to detect hepatic steatosis between FLI and TyG as well as the combination of TyG and obesity indices among postmenopausal women, and confirms that FLI is a superior indicator over TyG along or the combination of TyG and frequently used obesity indices. In addition, we only recruited relatively healthy women without diabetes, which avoids the potential influence of diabetes on metabolisms of the participants. Furthermore, we not only calculated the AUC values of FLI and TyG, but also compared the differences between them statistically, which enhances convincingness of our data. On the other side, the current study has several limitations. Its cross-sectional design makes it difficult to assess causal relationship. Also, we did not evaluate the level of insulin resistance as well as the blood estrogen level in each participant, thus, we could not provide any mechanistic explanation regarding our results. In addition, because all participants of this study, who were of Chinese ethnicity and were residents of Beijing, were enrolled in a single hospital and the sample size was relatively small, so our results cannot be extrapolated beyond this group. Further, ultrasonography as a modality for detecting NAFLD is not the gold standard for the diagnosis of NAFLD, but is generally regarded as a fairly noninvasive and reliable modality for the diagnosis of hepatic steatosis, with a known sensitivity of 85% and specificity of 94% [57]. Finally, we were unable to collected detailed data about diet and physical activity and so on.