Experimental Gerontology
journal homepage: www.elsevier.com/locate/expgero
The associations between liver enzymes and the risk of metabolic syndrome T
in the elderly
⁎
Cun-Fei Liua,b, Wei-Ning Zhouc, Zheng Lua, Xue-Ting Wanga, Zhao-Hui Qiua,
a
Department of Cardiology, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200336, China
b
Department of Cardiology, Linyi People's Hospital, Linyi, Shandong 276000, China
c
Department of Pathology, East Hospital, Tongji University School of Medicine, Shanghai 200120, China
A R T I C LE I N FO A B S T R A C T
Section Editor: Holly M. Brown-Borg Background: Studies have demonstrated that liver enzymes are associated with metabolic syndrome (MetS).
Keywords: However, little information is available regarding these relationships in elderly populations. Our present study
Liver enzyme aimed to explore the associations between liver enzymes and the risk of MetS in elderly populations.
Metabolic syndrome Methods: This cross-sectional study included 1444 elder participants (970 men and 474 women) who attended
Elderly annual physical examinations. Univariate and multivariate logistic regressions were performed to estimate the
associations between liver enzymes and the risk of MetS and its components according to quartiles of the
concentration of each liver enzyme.
Results: The prevalence of MetS and its components increased remarkably with increasing quartiles of alanine
aminotransferase (ALT), gamma-glutamyltransferase (GGT) and alkaline phosphatase (ALP) but not with as-
partate aminotransferase (AST) in the elderly. Compared with subjects in the bottom quartile, the adjusted odds
ratio for MetS in the highest ALT, GGT and ALP quartiles were 1.78 (95% CI 1.21–2.61), 2.58 (95% CI
1.77–3.78) and 1.85 (95%CI 1.27–2.70) respectively. No statistically significant increases in the odds ratio for
MetS according to increased quartiles of AST were found in either the univariate or multivariate logistic re-
gression analyses.
Conclusions: Elevated liver enzymes levels (mainly ALT, GGT and ALP but not AST) are positively associated
with the prevalence of MetS in elderly populations.
⁎
Corresponding author.
E-mail address: QCH3503@shtrhospital.com (Z.-H. Qiu).
https://doi.org/10.1016/j.exger.2018.02.026
Received 19 August 2017; Received in revised form 28 October 2017; Accepted 25 February 2018
Available online 27 February 2018
0531-5565/ © 2018 Published by Elsevier Inc.
C.-F. Liu et al. Experimental Gerontology 106 (2018) 132–136
2. Methods Table 1
Characteristics of the study populations.
2.1. Study populations
MetS(n = 524) Non-MetS(n = 920) P value
The present cross-sectional study enrolled 1680 Han Chinese elderly Sex (men, %) 358 (68.32%) 612 (66.52%) 0.484
participants (aged 60–93 years) who visited the health examination Age (year) 69.58 ± 7.01 70.04 ± 7.65 0.255
BMI (kg/m2) 26.81 ± 2.60 23.30 ± 2.83 < 0.001
center of Tongren hospital for annual physical check-ups from March
WC (cm) 93.16 ± 10.62 80.81 ± 11.26 < 0.001
2016 to October 2016. All participants completed a health ques- Current smoking (%) 26 (4.96%) 59 (6.41%) 0.616
tionnaire and health check-up according to a standardized protocol. SBP (mm Hg) 139.02 ± 16.23 130.67 ± 17.23 < 0.001
Because serum liver enzyme levels can be significantly affected by al- DBP (mm Hg) 82.51 ± 10.31 78.02 ± 9.66 < 0.001
cohol consumption and hepatitis viruses, those who were currently TG (mg/dl) 217.75 ± 135.10 127.72 ± 83.10 < 0.001
TC (mg/dl) 201.11 ± 41.20 196.37 ± 36.78 0.024
drinking and those who were currently suffering from viral hepatitis
HDL-C (mg/dl) 58.18 ± 15.92 69.35 ± 17.37 < 0.001
were excluded from our present study. Ultimately, 1444 elderly parti- LDL-C (mg/dl) 102.81 ± 31.63 99.48 ± 27.93 0.039
cipants (970 men and 474 women) with complete data were included in FPG (mmol/L) 6.31 ± 1.97 5.35 ± 1.21 < 0.001
our study. Written informed consent was obtained from all eligible ALT (IU/L) 26.98 ± 15.51 22.01 ± 12.58 < 0.001
AST (IU/L) 23.37 ± 8.85 23.25 ± 8.66 0.796
participants, and this study was approved by the Ethics Committee of
GGT (IU/L) 29.80 ± 19.54 23.42 ± 18.93 < 0.001
Tongren Hospital, Shanghai Jiao Tong University School of Medicine. ALP (IU/L) 86.25 ± 16.25 81.41 ± 12.80 < 0.001
Total bilirubin 14.50 ± 5.27 14.65 ± 5.53 0.617
2.2. Data collection and laboratory measurements Albumin 37.01 ± 4.31 36.98 ± 4.13 0.906
Uric acid (mg/dl) 6.26 ± 1.52 5.67 ± 1.36 < 0.001
Creatinine (umol/l) 81.48 ± 25.71 80.16 ± 24.25 0.331
A standardized questionnaire was used to obtain the general in-
No of MetS components 3.31 ± 0.46 1.38 ± 0.68 < 0.001
formation of the subjects, including age, medical history, history of
drug treatment, cigarette smoking, etc. Standing height and weight Abbreviation: BMI: body mass index; WC: waist circumference; TG: triglyceride; TC: total
were measured without shoes to the nearest 0.1 cm and 0.1 kg, re- cholesterol; HDL-C: high-density lipoprotein cholesterol; LDL-C: low-density lipoprotein
spectively. Waist circumference (WC) was measured to the nearest cholesterol; FPG: fasting plasma glucose; ALT: alanine aminotransferase; AST: aspartate
0.1 cm between iliac crest and the rib cage with a non-elastic tape. The aminotransferase; GGT: gamma-glutamyltransferase. ALP: alkaline phosphatase.
body mass index (BMI) was assessed by the formula weight (kg)/
height2 (m2). Resting blood pressure was measured two times with an levels. All statistical tests were two-sided, and a P-value < 0.05 was
electronic sphygmomanometer (HEM-741C; Omron, Tokyo, Japan) in considered to be statistically significant. All statistical analyses were
the seated position after at least 5 min of rest in a quiet room. performed with SPSS software 18.0 (SPSS Inc., Chicago, IL, USA).
Venous blood samples after an overnight fast were obtained from
the antecubital vein and were then sent to the laboratory center for 3. Results
analysis. Fasting plasma glucose (FPG), total cholesterol (TC), high-
density lipoprotein cholesterol (HDL-C), low-density lipoprotein cho- 3.1. Characteristics of the study populations
lesterol (LDL-C), triglycerides (TG), creatinine, uric acid and liver en-
zymes were measured enzymatically on an automatic analyzer The main characteristics of subjects are presented in Table 1.
(Architect Ci8200, Abbott Co., Illinois, USA). All laboratory assays were Among the included 1444 participants, 524 subjects were diagnosed
measured without knowledge of the information of the participants. with MetS, and the prevalence of MetS was 36.3% across all subjects
(35.0% of the women and 36.9% of the men). There were no significant
2.3. Definition of MetS differences in age, gender or smoking status between the MetS and non-
MetS groups (P > 0.05). However, the subjects in MetS group had
In our present study, we chose the definition of MetS according to significantly higher WC, BMI, SBP, DBP, TC, TG, LDL-C, FPG, and uric
the 2009 harmonizing definition criteria as including three or more of acid levels but lower HDL-C values than the subjects in the non-MetS
the following factors (Alberti et al., 2009): abdominal obesity, i.e., groups. Additionally, the mean number of MetS components was much
WC ≥ 90 cm in Asian men or ≥80 cm in Asian women; systemic hy- higher in the MetS group than non-MetS group (3.31 ± 0.46 vs
pertension, i.e., a systolic blood pressure (SBP) ≥ 130 mm Hg, a dia- 1.38 ± 0.68; P < 0.01).
stolic blood pressure (DBP) ≥ 85 mm Hg, or the use of antihypertensive
drugs; hypertriglyceridemia, i.e., TG ≥ 150 mg/dl; reduced HDL-C, i.e., 3.2. Correlations of liver enzyme levels and MetS components
HDL-C < 40 mg/dl in men or < 50 mg/dl in women; hyperglycemia,
i.e., FPG ≥ 100 mg/dl or the use of antidiabetic agents. Pearson's correlation coefficients were calculated to evaluate the
correlations between liver enzyme levels and MetS components after
2.4. Statistical analysis adjustments for sex and age (Table 2). ALT was positively associated
with WC, FPG and TG and negatively correlated with HDL-C. GGT was
Continuous variables are summarized as the means with the stan- positively correlated with WC, FPG, TG, SBP and DBP. ALP was posi-
dard deviations (SDs), and categorical variables are expressed as the tively associated with WC, FPG and TG and negatively correlated with
numbers and percentages. Independent t-tests and chi-square tests were HDL-C. However, there were no statistically positive or negative cor-
used to compare the differences in characteristics difference between relations of AST with any MetS components.
the MetS group and non-MetS group. To evaluate the odds ratio (ORs)
for MetS according to varying levels of liver enzymes, the subjects were 3.3. Odds ratios for MetS according to the quartiles of the liver enzyme
divided into quartiles according to their liver enzymes levels. Pearson's levels
correlation coefficients were used to calculate the associations of liver
enzyme levels with each component of MetS. Univariate and multi- Univariate and multivariate logistic regression analyses were con-
variate logistic regression were performed to evaluate the ORs of MetS ducted to evaluate the liver enzyme levels and the risk of MetS. As
and its components according to the quartiles of the liver enzymes presented in Table 3, compared with the subjects in the bottom ALT
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C.-F. Liu et al. Experimental Gerontology 106 (2018) 132–136
Table 2
Correlation coefficients between liver enzyme and each MetS component.
Pearson's coefficients P value Pearson's coefficients P value Pearson's coefficients P value Pearson's coefficients P value
WC 0.190 < 0.001 −0.008 0.751 0.128 < 0.001 0.169 < 0.001
FPG 0.150 < 0.001 −0.004 0.890 0.090 0.001 0.140 < 0.001
SBP 0.012 0.654 −0.021 0.420 0.080 0.002 0.004 0.866
DBP 0.025 0.347 0.000 0.985 0.102 < 0.001 0.028 0.289
TG 0.119 < 0.001 0.025 0.352 0.184 < 0.001 0.105 < 0.001
HDL-C −0.097 < 0.001 0.042 0.113 −0.045 0.087 −0.099 < 0.001
Abbreviation: ALT: alanine aminotransferase; AST: aspartate aminotransferase; GGT: gamma-glutamyltransferase; ALP: alkaline phosphatase; WC: waist circumference; FPG: fasting
plasma glucose; SBP: systolic blood pressure; DBP: diastolic blood pressure; TG: triglyceride; HDL-C: high-density lipoprotein cholesterol.
quartile, the unadjusted OR of the MetS patients increased from 1.37 trend = 0.868). ALT was positively associated with increased ORs for
(95% CI 0.99–1.88) for the second quartile group to 3.17 (95% CI all MetS components except hypertension (1.43 (95% CI 0.99–2.06),
2.30–4.36) for the highest quartile group (P for trend < 0.001), and P = 0.127). GGT was positively associated with increased ORs for all
the OR increased from 1.23 (95% CI 0.89–1.72) to 3.75 (95% CI MetS components, including central obesity, dyslipidemia, hypergly-
2.75–5.12) across the GGT quartiles (P for trend < 0.001). As to ALP, cemia and hypertension. ALP was positively associated with increased
the unadjusted OR of the MetS increased from 1.07 (95% CI 0.77–1.48) ORs for all MetS components but not with hypertension (1.21 (95% CI
for the second quartile group to 2.75 (95% CI 2.01–3.77) for the highest 0.83–1.76), P = 0.316). However, no significant positive associations
quartile group (P for trend < 0.001). The ORs for MetS were atte- between the AST levels and any of the MetS components were found.
nuated, but they remained significant after adjustments for several
covariates (i.e., age, sex, BMI, current smoking, uric acid and creati-
nine) in regard ALT, GGT and ALP levels. The adjusted OR for the 4. Discussion
highest quartiles of ALT, GGT and ALP were 1.78 (95% CI 1.21–2.61),
2.58 (95% CI 1.77–3.78) and 1.85 (95%CI 1.27–2.70) respectively. The prevalence of MetS is increasing with the economic and social
However, no statistically significant increase in the risk of MetS ac- development in the world and much more common in the elderly
cording to increased concentrations of AST was found in either the people. For example, the incidence of MetS has been reported to be
univariate or multivariate logistic regression analyses. 21.3% in the China Health and Nutrition Survey according to NCEP
ATPIII criteria, but the prevalence of MetS is dramatically increased to
36.7% among elderly people (60 years or older) (Xi et al., 2013).
3.4. Association between liver enzymes concentration and each component Moreover, the risk of MetS in elderly populations is 4.41 times higher
of MetS (95%CI 3.69–5.29) than that in people < 40 years old (Xi et al., 2013).
In our present study, we investigated the association between hepatic
We further investigated the association between liver enzymes and enzyme concentrations and the risk of MetS in elderly people. Our re-
the risk of MetS components after adjustments for age and sex. The sults revealed that elevated ALT, GGT and ALP concentrations were
detailed results are provided in Table 4. Generally, the prevalence of positively associated with MetS and its components in elderly subjects.
MetS components increased from the bottom quartiles to the highest Compared with the subjects in the bottom quartiles of ALT, GGT and
quartiles of ALT, GGT and ALP (P for trends < 0.05) with the exception ALP, the unadjusted ORs for MetS were 3.17 (95% CI 2.30–4.36), 3.75
of hypertension prevalence in ALT (P for trend = 0.593) and ALP (P for (95% CI 2.75–5.12) and 2.75 (95% CI 2.01–3.77), respectively, in the
Table 3
Odds ratios (95% CIs) of MetS according to quintiles of each liver enzyme.
Q1 Q2 Q3 Q4 P for trend
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C.-F. Liu et al. Experimental Gerontology 106 (2018) 132–136
Table 4
Age and sex adjusted odds ratios (95% CIs) of each MetS component according to quintiles of each liver enzyme.
Q1 Q2 Q3 Q4 P for trend
highest quartile groups. The ORs for MetS according to ALT, GGT and because it can also be secreted by other organs and cells, such as the
ALP levels were attenuated but remained significant after adjustments heart, skeletal muscle, kidneys, pancreas, lungs, leukocytes, and ery-
for several covariates (age, sex, BMI, current smoking, uric acid and throcytes (Pratt and Kaplan, 2000), and this may partially explain why
creatinine). However, no significant associations were found between no significant associations were found between MetS and AST in our
the AST level and MetS or MetS components. present study. The exact mechanisms that link liver enzymes with MetS
Liver enzymes have been widely explored as markers of MetS and its are still not fully understood. Possible explanations are described
components among different populations (Koskinen et al., 2012; Lee below. Elevated ALT, GGT and ALP are closely associated with liver fat
and Yang, 2013; Villegas et al., 2011). However, these studies have deposition (Clark et al., 2003) and are considered to be biomarkers of
provided inconsistent results. For example, Koskinen et al. (2012) found NAFLD (Hossain et al., 2016; Pantsari and Harrison, 2006; Schindhelm
no association between increased enzyme levels (mainly ALT and GGT) et al., 2006), whereas NAFLD is considered to be a mediator of MetS
and the atherogenicity of MetS in young adults. Villegas et al. (2011) (den Boer et al., 2004) and insulin resistance, and abdominal obesity
found that elevated ALT and AST were associated with the prevalence may be a pathophysiological distinction between NAFLD and MetS
of MetS in middle-aged Chinese men. Lee and Yang (2013) demon- (Bugianesi et al., 2010; Finucane et al., 2014). Moreover, studies have
strated that ALT and GGT were associated with MetS in adolescents. demonstrated that ALT and GGT are also positively associated with
Hanley et al. (2005) showed significant cross-sectional associations of insulin resistance and MetS in obese subjects (Marchesini et al., 2005;
ALT and ALP with MetS in American aged 40–69 years. Our present Wallace et al., 2007).
study revealed that elevated ALT, GGT and ALP were positively asso- Several limitations of our present study should be noted. First, our
ciated with MetS in an elderly population. Based on the above research study design was cross-sectional; therefore, we are unable to elucidate
results, it seems that age might be an influential factor in the associa- causal relationships between liver enzymes and MetS. However, the
tion of liver enzymes with the incidence of MetS. Indeed, there are available studies in general adults indicate that elevated liver enzymes
significant different liver enzymes levels when the elderly subjects were may be a predictor of the future development of MetS (Goessling et al.,
further grouped according to quintiles of age (data was shown in sup- 2008; Nakanishi et al., 2004). Second, the single measurements of he-
plemental material). patic enzyme concentrations may have led to some misclassifications of
ALT is regarded as the most specific biomarker of hepatic function the subjects, but several prospective studies have confirmed that
and is used as an indirect marker of liver injury. GGT is an enzyme that longitudinal increases in the liver enzymes are positively associated
is involved in the extracellular catabolism of the antioxidant glu- with MetS (Patel et al., 2007; Ryu et al., 2010). Finally, we adjusted for
tathione and is thought to be a marker of oxidative stress and sub- several potential confounding factors during our evaluations of the
clinical inflammation (Anderson et al., 1982; Lee et al., 2004). ALP is associations of liver enzymes with MetS in our statistical models;
responsible for hydrolysis of phosphate esters and is a biomarker for however, residual confounding effects may still exist.
liver function. However, AST is a less specific marker of liver injury
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C.-F. Liu et al. Experimental Gerontology 106 (2018) 132–136
5. Conclusion Koskinen, J., Magnussen, C.G., Kahonen, M., Loo, B.M., Marniemi, J., Jula, A., Saarikoski,
L.A., Huupponen, R., Viikari, J.S., Raitakari, O.T., Juonala, M., 2012. Association of
liver enzymes with metabolic syndrome and carotid atherosclerosis in young adults.
In summary, our present study demonstrated that elevated ALT, The cardiovascular risk in young Finns study. Ann. Med. 44 (2), 187–195.
GGT and ALP levels are positively associated with the prevalence of Kotronen, A., Yki-Jarvinen, H., 2008. Fatty liver: a novel component of the metabolic
MetS in an elderly population. Because ALT, GGT and ALP are closely syndrome. Arterioscler. Thromb. Vasc. Biol. 28 (1), 27–38.
Lee, K., Yang, J.H., 2013. Which liver enzymes are better indicators of metabolic syn-
related to NAFLD, further random control trials are needed to elucidate drome in adolescents: the Fifth Korea National Health and Nutrition Examination
the influence of treating NAFLD on the prevalence of MetS. Survey, 2010. Metab. Syndr. Relat. Disord. 11 (4), 229–235.
Lee, D.H., Blomhoff, R., Jacobs Jr., D.R., 2004. Is serum gamma glutamyltransferase a
marker of oxidative stress? Free Radic. Res. 38 (6), 535–539.
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