Journal of Diabetes 10 (2018), 641–652

ORIGINAL ARTICLE

Utility of three novel insulin resistance-related lipid

indices for predicting type 2 diabetes mellitus among
people with normal fasting glucose in rural China

Highlights
• Data are limited regarding the prevention of type 2 diabetes mellitus (T2DM) in rural Chinese people.
• Elevated triglyceride glucose, visceral adiposity, and lipid accumulation product are significantly associated
with the risk of incident T2DM.
• Triglyceride glucose, visceral adiposity, and lipid accumulation product did not improve the T2DM prediction
compared with fasting plasma glucose or waist circumference.

Bingyuan WANG,1 Ming ZHANG,2 Yu LIU,3 Xizhuo SUN,3 Lu ZHANG,1 Chongjian WANG,1 Linlin LI,1
Yongcheng REN,1,2,3 Chengyi HAN,1,2,3 Yang ZHAO,1,2,3 Junmei ZHOU,2,3 Chao PANG,4 Lei YIN,4
Tianping FENG,4 Jingzhi ZHAO4 and Dongsheng HU1
1
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, China, 2Department of
Preventive Medicine, Shenzhen University Health Science Center, Shenzhen, China, 3The Affiliated Luohu Hospital of Shenzhen University
Health Science Center, Shenzhen, China, and 4Department of Prevention and Health Care, Military Hospital of Henan Province, Zhengzhou,
China

Correspondence
Dongsheng Hu, Department of
Epidemiology and Health Statistics,
College of Public Health, Zhengzhou
University, 100 Kexue Avenue,
Zhengzhou, Henan 450001, China.
Tel: +86 371 6778 1963
Fax: +86 371 8667 1963
Email: dongsheng_hu@zzu.edu.cn
Received 10 July 2017; revised 17
December 2017; accepted 7
January 2018.
doi: 10.1111/1753-0407.12642
Abstract
Background: Inexpensive and easily measured indices are needed for the early
prediction of type 2 diabetes mellitus (T2DM) in rural areas of China. The aim
of this study was to compare triglyceride glucose (TyG), visceral adiposity
(VAI), and lipid accumulation product (LAP) with traditional individual mea-
sures and their ratios for predicting T2DM.
Methods: Data for 11 113 people with baseline normal fasting glucose in a
rural Chinese cohort were followed for a median of 6.0 years. Cox propor-
tional hazards regression was used to calculate covariate-adjusted hazard ratios
(aHRs) and 95% confidence intervals (95% CIs) and receiver operating charac-
teristic analysis was used to compare the ability of traditional measures and
TyG, VAI, and LAP at baseline to predict T2DM at follow-up.
Results: Among individual measures, fasting plasma glucose (FPG) and waist
circumference (WC) were strongly associated with T2DM. Of all lipid ratios, an
elevated triglycerides (TG) to high-density lipoprotein cholesterol (HDL-C)
ratio was associated the most with T2DM. Compared with the first quartiles of
TyG, VAI, and LAP, their fourth quartiles were associated with T2DM for men
(aHR 3.54 [95% CI 2.08–6.03], 2.89 [1.72–4.87], and 5.02 [2.85–8.85], respec-
tively) and women (6.15 [3.48–10.85], 4.40 [2.61–7.42], and 6.49 [3.48–12.12],
respectively). For predicting T2DM risk, TyG, VAI, and LAP were mostly supe-
rior to the TG: HDL-C ratio, but did not differ from FPG and WC.
Conclusions: Prediction of T2DM was not improved by TyG, VAI, and LAP
versus FPG or WC alone. Therefore, TyG, VAI, and LAP may not be inex-
pensive tools for predicting T2DM in rural Chinese people.
Keywords: cohort study, diabetes, fat accumulation, insulin resistance, lipid
index.

© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd 641
Diabetes prevention in China
Introduction
China is home to the largest number of adults living
with type 2 diabetes mellitus (T2DM) worldwide.1 In
the latest national survey of China in 2010, although
the prevalence of T2DM was lower for rural than urban
residents (10.3% vs 14.3%), that of prediabetes was
greater for rural than urban residents (50.9% vs 48.4%),
and the rates were lower for rural than urban residents
for awareness (24.6% vs 38.7%), treatment (21.5% vs
32.7%), and control (38.6% vs 40.8%) of T2DM.2 Fur-
thermore, household income and health care expendi-
ture are lower in rural than urban areas of China.3 In
terms of the epidemic state of T2DM for rural residents,
the situation will be grim if we do not establish immedi-
ate control measures. Therefore, we must explore inex-
pensive and easily measurable indices for the early
prediction of T2DM in rural areas.
Insulin resistance (IR) and/or visceral adiposity are
well-known risk factors for T2DM in the general popu-
lation.4 People with T2DM often show prior impaired
fasting glucose and features of IR.5 In addition, ectopic
fat deposition in the abdominal viscera and liver can
result in inflammatory and adipokine dysregulation, as
well as IR, which may accelerate the development of
T2DM.6 For these reasons, identifying IR and visceral
adiposity can be helpful in the primary and secondary
prevention of T2DM.
The hyperinsulinemic–euglycemic clamp is considered
the gold standard to define IR,7 and imaging techniques
such as magnetic resonance imaging and computed
tomography can measure fat distribution and quantify
adiposity accurately.8 However, none of these tech-
niques is cheap or can be used in large epidemiological
studies. Thus, we need indicators that are easily mea-
sured and widely applicable with a high ability to pre-
dict to T2DM for the general population.
Several studies have reported using the triglyceride
glucose (TyG) index, the product of triglycerides
(TG) and fasting plasma glucose (FPG) levels, as a sur-
rogate measure to identify IR.9 Compared with the
hyperinsulinemic–euglycemic clamp, TyG showed high
sensitivity (96.5%) and specificity (85%) for the diagno-
sis of IR in Mexican people.9 In addition, previous
studies proposed another two reliable lipid indices to
estimate IR from visceral adiposity dysfunction, one
being the visceral adiposity index (VAI), based on body
mass index (BMI), waist circumference (WC), TG and
high-density lipoprotein cholesterol (HDL-C) levels,10,11
and the other being the lipid accumulation product
(LAP), which is calculated from WC and fasting TG
levels.12 Several studies have reported significant associ-
ations between TyG, VAI, LAP, and T2DM.4,13–18
642 © 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
B. WANG et al.
However, the ability of TyG and VAI to predict T2DM
incidence is contentious compared with that of other
fatness indices.4,14–16,18 In addition, there are limited
data regarding the association between LAP and diabe-
tes.17 These indices should be validated in different eth-
nic groups.
Therefore, in the present study we conducted a
population-based prospective cohort study of rural Chi-
nese participants with normal FPG at baseline to:
(i) evaluate the relationship between the TyG, LAP,
and VAI indices and risk of incident T2DM; and
(ii) compare the ability of TyG, LAP, VAI, and both
traditional individual measures (FPG, WC, total choles-
terol [TC], TG, HDL-C, low-density lipoprotein choles-
terol [LDL-C]) and lipid ratios (TG: HDL-C,
TC: HDL-C, TC: LDL-C, and LDL-C: HDL-C
ratios) to predict the risk of incident T2DM.
Methods
Study population
Between July–August 2007 and July–August 2008,
20 194 participants age ≥ 18 years were recruited using
a cluster sampling method from a rural Chinese popula-
tion in Henan province and underwent baseline exami-
nations; of these, 17 265 were re-examined in July–
August 2013 and July–October 2014 (response rate
85.5%). Details of the study design and characteristics
of the study population have been described
elsewhere.19–21 Participants were excluded from the
study if they: (i) had T2DM (n = 1302) or type 1 diabe-
tes mellitus (n = 13) at baseline; (ii) had impaired fast-
ing glucose (IFG; FPG 6.1–6.9 mmol/L;22 n = 1122) or
unknown diabetic status (n = 10) at baseline; or
(iii) had died (n = 1110) or did not have biochemical
data (n = 2583) during follow-up. Those who did not
have biochemical data primarily because they had
moved to another place were investigated by telephone
follow-up. The final sample for the present analysis con-
sisted of 11 113 people with baseline normal fasting glu-
cose (6844 women).
This study was approved by the Shenzhen University
Medical Ethics Committee. All procedures were per-
formed in accordance with the ethical standards of the
responsible committee on human experimentation and
with the 1975 Declaration of Helsinki and its later
amendments.
Data collection and measurements
Data were collected in examination centers at local
health stations or in community clinics in the
B. WANG et al. Diabetes prevention in China

participants’ residential areas. Participants who were VAI, and LAP were calculated using the following
unable to attend the examination center were examined formulas:
in their home. Trained research staff administered a
standard questionnaire to collect information on sex, TyG = ln ðTG × FPG=2Þ:
age, education level, marital status, smoking status,
alcohol intake, and physical activity. Participants who with TG and FPG both in mg/dL.9
had not smoked >100 cigarettes in their lifetime were    
considered never-smokers; the others were considered WC TG
VAI ðmenÞ = ×
smokers. Drinkers were defined as those who reported 39:68 + ð1:88 × BMIÞ 1:03
 
consuming alcohol >12 times in the previous 1:31
×
12 months. Physical activity level was classified using HDL − C
the short version of the International Physical Activity    
WC TG
Questionnaire23 into one of three levels: VAI ðwomenÞ = ×
36:58 + ð1:89 × BMIÞ 0:81
1. Low physical activity: individuals who did not meet  
1:52
the criteria for the two other categories. ×
2. Moderate physical activity: individuals meeting one HDL − C
of the following three criteria:
• ≥3 days/week of vigorous-intensity activity of at with WC in cm, BMI in kg/m2, and TG and HDL-C
least 20 min/day. both in mmol/L.10
• ≥5 days/week of moderate-intensity activity and/or
walking at least 30 min/day. LAP ðmenÞ = ðWC – 65Þ × TG
• ≥5 days/week of any combination of walking, LAP ðwomenÞ = ðWC – 58Þ × TG
moderate-intensity or vigorous-intensity activities
achieving a total score of at least 600 metabolic with WC in cm and TG in mmol/L.26
equivalent (MET)
min/week. Data collection at follow-up was the same as at the
3. High physical activity: Individuals meeting one of baseline examination.
the following two criteria: Type 2 diabetes mellitus was defined as FPG ≥ 7.0
• Vigorous-intensity activity on at least 3 days/week mmol/L and/or the use of insulin or oral hypoglycemic
achieving a total score of at least 1500 agents, and/or a self-reported history of T2DM.22
MET
min/week
• ≥7 Days/week of any combination of walking, Statistical analysis
moderate-intensity or vigorous-intensity activities
achieving a total score of at least 3000 MET All continuous data are described as the median (inter-
min/week. quartile range) because of skewed distribution and were
Participants were asked to wear light clothes and be analyzed using the Wilcoxon rank sum test. Categorical
barefoot when anthropometric indices were measured. data are presented as percentages and were analyzed
Height and weight were measured by trained investigators using the Chi-squared test. Fasting plasma glucose,
under standardized conditions following a standard pro- WC, TC, TG, HDL-C, LDL-C, TG: HDL-C, TC:
tocol. In standing participants, WC was measured mid- HDL-C, TC: LDL-C, LDL-C: HDL-C ratios, and
way between the lower edge of the costal arch and the TyG, VAI, and LAP indices were categorized into
upper edge of the iliac crest. Participants were measured quartiles. A Cox proportional hazard regression model
twice, and the average was used. Blood pressure was mea- was used to estimate hazard ratios (HRs) and 95% con-
sured using an electronic sphygmomanometer (HEM- fidence intervals (CIs) for incident T2DM by quartile
770AFuzzy; Omron, Kyoto, Japan) after at least a 5-min for each individual measure, lipid ratio, and the TyG,
rest, with participants in a seated position, according to VAI, and LAP indices. The HRs and 95% CIs for the
the American Heart Association standardized protocol.24 upper three quartiles were calculated using the lowest
The measurements were repeated three times at 30-s inter- quartile as the reference category. Two models were
vals, and the average was used for analysis. fitted: Model 1, controlling for age, family history of
Blood samples were obtained after an overnight fast diabetes, and family history of hypertension; and Model
of at least 8 h. Levels of FPG, TG, TC, and HDL-C 2, additionally adjusted for education level, marital sta-
were measured using an automatic clinical analyzer tus, smoking, alcohol consumption, physical activity,
(Model 7060; Hitachi, Tokyo, Japan). The LDL-C level and systolic blood pressure (SBP). The linear trends
was calculated using the Friedewald formula;25 TyG, across FPG, WC, TG: HDL-C ratio, TyG, VAI, and

© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd 643
Diabetes prevention in China
LAP quartiles were evaluated by a median value within
each quartile used as a continuous variable. The area
under the receiver operating characteristic (ROC) curve
(AUC) was used to test the ability of FPG, WC, TG:
HDL-C ratio, and TyG, VAI and LAP indices at base-
line to predict the risk of T2DM at follow-up. Differ-
ences in AUCs were compared by a non-parametric test
developed by DeLong et al.27 There were no missing
data for the main outcome variables. The ROCs were
calculated using STATA v12.0 (StataCorp, College Sta-
tion, TX, USA) and other analyses were performed
using SAS 9.1 (SAS Institute, Cary, NC, USA). Two-
sided P < 0.05 was considered significant.
Results
During a median of follow-up of 6.0 years, T2DM
developed in 439 people; the overall incidence of
T2DM was 6.59/1000 person-years. The T2DM inci-
dence for men and women was 7.29 and 6.14/1000
person-years, respectively. Table 1 summarizes the base-
line characteristics of participants according to T2DM
status at follow-up and by sex.
For men, a family history of diabetes was more fre-
quent with than without T2DM (P < 0.001). Type 2 dia-
betes mellitus was associated with increased BMI, WC,
SBP, DBP, FPG, TC, TG, TG: HDL-C, TC: HDL-
C, and LDL-C: HDL-C ratios, and TyG, VAI, and
LAP values, but reduced HDL-C levels (all P < 0.05).
For women, T2DM was associated with older age,
increased BMI, WC, SBP, DBP, FPG, TC, TG, LDL-
C, TG: HDL-C, TC: HDL-C, and LDL-C: HDL-C
ratios, and TyG, VAI, and LAP values, but reduced
HDL-C levels (all P < 0.05).
After adjusting for variables in Model 2, the risk of
incident T2DM was increased with elevated FPG, WC,
TC, TG, TG: HDL-C and TC: HDL-C ratios, and
TyG, VAI, and TyG values for both men and women
(Fig. 1). Compared with other individual measures, high
FPG was associated the most with T2DM for both men
(adjusted [a] HR 5.96, 95% CI 3.48–10.23; χ2 = 42.07,
P < 0.001) and women (aHR 5.05, 95% CI 3.18–8.03;
χ2 = 47.00, P < 0.001). A strong association between
WC and T2DM was observed among both men (aHR
4.25, 95% CI 2.51–7.21; χ2 = 28.85, P < 0.001) and
women (aHR 4.07, 95% CI 2.36–7.03; χ2 = 25.49,
P < 0.001). Compared with other lipid ratios, the TG:
HDL-C ratio was associated the most with T2DM for
both men (aHR 2.37, 95% CI 1.45–3.86; χ2 = 11.91,
P = 0.001) and women (aHR 4.05, 95% CI 2.46–6.67;
χ2 = 30.33, P < 0.001). Receiver operating characteristic
analysis revealed similar results (data not shown).
644 © 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
B. WANG et al.
Therefore, we compared TyG, VAI, and LAP indices,
FPG, WC, and the TG: HDL-C ratio to explore
whether TyG, VAI, and LAP could improve the ability
to predict incident T2DM.
The incidence of T2DM by quartiles of TyG, VAI,
and LAP was increased for men (Table 2) and women
(Table 3; Ptrend < 0.001 for all). For men, the risk of
incident T2DM was increased with Quartiles 3 and 4 of
TyG versus Quartile 1 (aHR 2.22 [95% CI 1.27–3.88;
χ2 = 7.92, P < 0.01] and aHR 3.54 [95% CI 2.08–6.03;
χ2 = 21.67, P < 0.001], respectively), but only with
Quartile 4 (vs Quartile 1) of VAI (aHR 2.89, 95% CI
1.72–4.87; χ2 = 16.02, P < 0.001) and with Quartiles
3 and 4 (vs Quartile 1) of LAP (aHR 2.12 [95% CI
1.15–3.91; χ2 = 5.75, P = 0.02] and aHR 5.02 [95% CI
2.85–8.85; χ2 = 31.04, P < 0.001], respectively).
The risk of T2DM was even greater for women than
men with increasing quartiles of TyG, VAI, and LAP.
The risk of T2DM was increased with Quartiles 2–4 of
TyG versus Quartile 1 (aHR 2.50 [95% CI 1.36–4.60;
χ2 = 8.67, P < 0.01], aHR 3.12 [95% CI 1.72–5.67;
χ2 = 14.00, P < 0.001], and aHR 6.15 [95% CI
3.48–10.85; χ2 = 39.25, P < 0.001], respectively) and
Quartiles 3 and 4 of VAI (aHR 2.13 [95% CI 1.22–3.74;
χ2 = 7.01, P = 0.01] and aHR 4.40 [95% CI 2.61–7.42;
χ2 = 31.00, P < 0.001], respectively). For LAP, the risk
of T2DM was increased with Quartiles 2–4 (aHR 2.42
[95% CI 1.23–4.74; χ2 = 6.59, P = 0.01], aHR 3.65
[95% CI 1.92–6.92; χ2 = 15.69, P < 0.001], and aHR
6.49 [95% CI 3.48–12.12; χ2 = 34.57, P < 0.001],
respectively).
The ROC curves and AUCs for FPG, WC, TG:
HDL-C ratio, and TyG, VAI, and LAP indices for dis-
criminating T2DM incidence by sex are shown in Fig. 2
and summarized in Table 4. All these indicators had
high negative predictive value but low positive predic-
tive value for predicting T2DM. In both men and
women, TyG, VAI, and LAP had a higher sensitivity
but lower specificity than FPG. For men, TyG had a
similar AUC as the TG: HDL-C ratio, FPG, and WC
(all P > 0.05). The AUCs for VAI and LAP were simi-
lar to those for FPG (all P > 0.05) and WC (all
P > 0.05), but larger than that for the TG: HDL-C
ratio (all P < 0.05). For women, the AUCs for TyG,
VAI, and LAP were similar to those for FPG (all
P > 0.05) and WC (all P > 0.05), but larger than that
for the TG: HDL-C ratio (all P < 0.05).
Discussion
In the present population-based prospective cohort
study, we compared three novel IR-related lipid indices
 B. WANG et al.

Table 1 Baseline characteristics of the study participants by sex and type 2 diabetes mellitus status at follow-up

Men (n = 4269) Women (n = 6844)

Total (n = 11 113) No T2DM (n = 4081) T2DM (n = 188) P-value No T2DM (n = 6593) T2DM (n = 251) P-value
Age (years) 50.00 (41.00, 59.00) 52.00 (43.00, 61.00) 53.00 (42.00, 60.00) 0.94 48.00 (40.00, 57.00) 53.00 (44.00, 60.00) <0.001
High school or above 1137 (10.23) 650 (15.93) 30 (15.96) 0.99 442 (6.70) 15 (5.98) 0.65
Married or cohabiting 10 230 (92.08) 3713 (91.05) 177 (94.15) 0.14 6108 (92.64) 232 (92.43) 0.90
Smoking 3009 (27.08) 2863 (70.15) 130 (69.15) 0.77 14 (0.21) 2 (0.80) 0.11
Drinking alcohol 1247 (11.22) 1154 (28.28) 45 (23.94) 0.20 45 (0.68) 3 (1.20) 0.26
Physical activity
Low 5623 (50.60) 2407 (58.98) 102 (54.26) 0.21 2997 (45.46) 117 (46.61) 0.42
Moderate 2345 (21.10) 748 (18.33) 33 (17.55) 1515 (22.98) 49 (19.52)
High 3145 (28.30) 926 (22.69) 53 (28.19) 2081 (31.56) 85 (33.86)
Family history
Diabetes* 573 (6.30) 194 (5.89) 22 (14.77) <0.001 339 (6.20) 18 (9.42) 0.07
Hypertension* 3687 (38.84) 1293 (37.69) 61 (40.67) 0.46 2242 (39.27) 91 (44.61) 0.13
BMI (kg/m2) 23.91 (21.62, 26.37) 23.13 (21.08, 25.44) 25.52 (22.29, 27.68) <0.001 24.27 (21.95, 26.81) 25.92 (23.85, 28.73) <0.001
WC (cm) 81.30 (74.50, 88.75) 81.50 (74.90, 89.25) 89.18 (79.50, 96.28) <0.001 80.85 (74.00, 87.75) 87.50 (80.50, 93.75) <0.001
SBP (mmHg) 121.33 (111.67, 135.33) 122.00 (112.33, 133.67) 126.50 (115.50, 135.50) <0.01 120.67 (109.33, 135.67) 130.33 (117.33, 147.33) <0.001
DBP (mmHg) 77.00 (70.33, 85.33) 76.67 (70.33, 84.33) 79.67 (72.50, 85.33) <0.01 77.00 (70.33, 85.33) 83.33 (76.00, 91.67) <0.001
FPG (mmol/L) 5.25 (4.94, 5.56) 5.22 (4.91, 5.53) 5.45 (5.13, 5.76) <0.001 5.25 (4.95, 5.55) 5.55 (5.17, 5.84) <0.001
TC (mmol/L) 4.34 (3.8, 4.97) 4.24 (3.74, 4.85) 4.37 (3.84, 5.05) 0.03 4.39 (3.83, 5.04) 4.69 (4.18, 5.21) <0.001
TG (mmol/L) 1.32 (0.95, 1.90) 1.28 (0.94, 1.83) 1.56 (1.12, 2.22) <0.001 1.33 (0.94, 1.89) 1.81 (1.23, 2.57) <0.001
HDL-C (mmol/L) 1.14 (0.99, 1.32) 1.09 (0.95, 1.26) 1.04 (0.89, 1.17) <0.01 1.18 (1.03, 1.37) 1.13 (0.99, 1.31) <0.01
LDL-C (mmol/L) 2.50 (2.00, 3.00) 2.50 (2.00, 2.90) 2.50 (2.10, 3.10) 0.56 2.50 (2.10, 3.00) 2.60 (2.10, 3.10) 0.03
TG: HDL-C ratio 1.16 (0.77, 1.79) 1.18 (0.79, 1.82) 1.51 (1.00, 2.37) <0.001 1.12 (0.74, 1.73) 1.62 (0.99, 2.47) <0.001

© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
TC: HDL-C ratio 3.80 (3.22, 4.48) 3.90 (3.30, 4.56) 4.27 (3.54, 4.95) <0.001 3.71 (0.15, 4.38) 4.11 (3.54, 4.89) <0.001
TC: LDL-C ratio 1.72 (1.60, 1.89) 1.70 (1.57, 1.87) 1.71 (1.57, 1.91) 0.60 1.73 (1.61, 1.91) 1.75 (1.63, 1.97) 0.15
LDL-C: HDL-C ratio 2.17 (1.74, 2.66) 2.25 (1.81, 2.76) 2.32 (1.88, 2.97) 0.04 2.11 (1.70, 2.58) 2.27 (1.78, 2.82) <0.01
TyG 8.61 (8.26, 8.99) 8.60 (8.24, 8.95) 8.82 (8.45, 9.19) <0.001 8.62 (8.26, 8.99) 8.94 (8.54, 9.34) <0.001
VAI 1.83 (1.17, 2.93) 1.47 (0.96, 2.30) 1.98 (1.25, 3.08) <0.001 2.06 (1.34, 3.24) 3.06 (1.92, 4.71) <0.001
LAP 26.78 (13.79, 47.56) 20.50 (9.88, 39.35) 37.53 (17.12, 72.00) <0.001 29.83 (16.32, 50.62) 51.15 (31.80, 83.27) <0.001

Data are given as the median (interquartile range) or n (%).

BMI, body mass index; DBP, diastolic blood pressure; FPG, fasting plasma glucose; HDL-C, high-density lipoprotein cholesterol; LAP, lipid accumulation product; LDL-C, low-density lipopro-
tein cholesterol; SBP, systolic blood pressure; T2DM, type 2 diabetes mellitus; TC, total cholesterol; TG, triglycerides; TyG, triglyceride glucose index; VAI, visceral adiposity index; WC, waist
circumference. *Partial data deletion.
Diabetes prevention in China

645
Diabetes prevention in China B. WANG et al.

Figure 1 Risk of incident type 2 diabetes mellitus (T2DM) by quartiles of traditional individual measures, lipid ratios and three novel indices in
men and women separately. HR, hazard ratio; CI, confidence interval; FPG, fasting plasma glucose; WC, waist circumference; TC, total choles-
terol; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; TyG, triglyceride glucose index;
VAI, visceral adiposity index; LAP, lipid accumulation product. Data are adjusted for age, education level, marital status, smoking, alcohol con-
sumption, physical activity, family history of diabetes, family history of hypertension, and systolic blood pressure.

(TyG, VAI, and LAP) with traditional individual mea-
sures and their ratios to predict T2DM in a rural Chi-
nese population. Elevated FPG, WC, TC, TG levels,
TG: HDL-C ratio, TC: HDL-C ratio, TyG, VAI, and
LAP were significantly associated with the risk of inci-
dent T2DM in both sexes. Fasting plasma glucose and
WC were superior to other individual measures for pre-
dicting T2DM, and the TG: HDL-C ratio was superior
to other lipid ratios for predicting T2DM in both men
and women. Compared with FPG, WC, and the TG:
HDL-C ratio, the AUCs for the three indices (TyG,
VAI, and LAP) were larger than that for the TG:
HDL-C ratio, but similar to those for FPG and WC.
The present study suggests that the TG: HDL-C and
TC: HDL-C ratios are significantly associated with
T2DM in both sexes, and an elevated TG: HDL-C
ratio is associated the most with T2DM, which is in
agreement with results from studies in other Chinese
populations.28,29 Nevertheless, the utility of these two
lipid ratios to identify T2DM in clinical practice is con-
troversial in different ethnic groups. In a multiethnic
study, the risk of IR was increased with an elevated
TG: HDL-C ratio in White obese subjects, but not in
Hispanics and African Americans.30 The main reason
for this finding may be differences in dietary and life-
style habits and metabolic-related indicators in different
ethnic groups,29,31 which could affect the association
between lipid ratios and IR and diabetes. In addition,
the relationship between lipid ratios and diabetes differs
depending on the selected study population. Results
from the Isfahan Diabetes Prevention Study showed
that the TG: HDL-C and TC: HDL-C ratios were not
robust predictors of T2DM in first-degree relatives of
patients with T2DM after a 7-year follow-up.32 How-
ever, another cohort study of an Iranian population
suggested a significant association of TG: HDL-C and
TC: HDL-C ratios with incident T2DM among non-
T2DM participants over a median follow up of
6.4 years for both sexes.33 Heredity may be the key fac-
tor for T2DM development among first-degree relatives
of people with T2DM. These groups may have a high
propensity for T2DM developing at a younger age,
even with low BMI and WC and favorable lipid
levels,32 which may weaken the relationship between
lipid ratios and T2DM.
The TyG index, which combines TG and FPG levels,
has been used to identify IR and T2DM in many epide-
miological studies.9,12,13 Both TG and FPG levels are
independent risk factors for IR and T2DM.34,35 Pancre-
atic β-cell dysfunction is considered the most important
risk factor for T2DM.36 Prolonged exposure to high
amounts of free fatty acids is associated with TG accu-
mulation in islets,37 which may alter the function of
pancreatic β-cells, leading to T2DM.38 Long-term expo-
sure to abnormally high levels of glucose can lead to
T2DM because of toxic effects on pancreatic β-cells.39

646 © 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
 Table 2 Cox proportional hazards regression analysis of risk of incident type 2 diabetes mellitus by quartiles of fasting plasma glucose, triglycerides: high-density lipoprotein cholesterol ratio,
triglyceride glucose index, visceral adiposity index, and lipid accumulation product for men

Model 1 Model 2
2
No. cases No. person-years Incidence* HR (95% CI) χ P-value HR (95% CI) χ2 P-value
B. WANG et al.

Fasting plasma glucose

Q1 (<4.92 mmol/L) 26 6584.08 3.95 1 1
Q2 (4.92–5.22 mmol/L) 37 6506.17 5.69 1.95 (1.05–3.59) 4.52 0.03 1.89 (1.02–3.49) 4.12 0.04
Q3 (5.23–5.54 mmol/L) 40 6461.17 6.19 2.31 (1.27–4.22) 7.45 <0.01 2.24 (1.23–4.10) 6.88 <0.01
Q4 (≥5.55 mmol/L) 85 6249.08 13.60 6.23 (3.65–10.65) 44.83 <0.001 5.96 (3.48–10.23) 42.07 <0.001
Ptrend <0.001 <0.001 <0.001
Waist circumference
Q1 (<75.00 cm) 26 6341.17 4.10 1 1
Q2 (75.00–81.47 cm) 34 6521.58 5.21 1.05 (0.58–1.91) 0.02 0.88 1.06 (0.58–1.94) 0.03 0.86
Q3 (81.75–89.74 cm) 38 6462.33 5.88 1.39 (0.77–2.50) 1.21 0.27 1.49 (0.82–2.69) 1.72 0.19
Q4 (≥89.75 cm) 90 6468.42 13.91 3.65 (2.21–6.01) 25.72 <0.001 4.25 (2.51–7.21) 28.85 <0.001
Ptrend <0.001 <0.001 <0.001
TG: HDL-C ratio
Q1 (<0.79) 28 6442.25 4.35 1 1
Q2 (0.79–1.18) 37 6458.92 5.73 1.14 (0.66–1.97) 0.21 0.65 1.15 (0.66–2.00) 0.25 0.62
Q3 (1.19–1.83) 48 6434.25 7.46 1.37 (0.81–2.34) 1.36 0.24 1.42 (0.83–2.43) 1.64 0.20
Q4 (≥1.84) 74 6380.58 11.60 2.41 (1.49–3.91) 12.80 <0.001 2.37 (1.45–3.87) 11.91 <0.001
Ptrend <0.001 <0.001 <0.001
Triglyceride glucose index
Q1 (<8.25) 28 6533.75 4.29 1 1
Q2 (8.25–8.57) 33 6451.42 5.12 1.54 (0.85–2.78) 2.04 0.15 1.59 (0.88–2.88) 2.32 0.13
Q3 (8.58–8.95) 51 6423.00 7.94 2.19 (1.26–3.80) 7.71 <0.01 2.22 (1.27–3.88) 7.92 <0.01
Q4 (≥8.96) 75 6327.00 11.85 3.55 (2.10–5.99) 22.39 <0.001 3.54 (2.08–6.03) 21.67 <0.001
Ptrend <0.001 <0.001 <0.001
Visceral adiposity index
Q1 (<0.97) 24 6443.50 3.72 1 1

© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
Q2 (0.97–1.47) 42 6429.33 6.53 1.62 (0.93–2.83) 2.85 0.09 1.65 (0.94–2.89) 3.07 0.08
Q3 (1.48–2.34) 44 6450.42 6.82 1.45 (0.82–2.57) 1.65 0.20 1.49 (0.84–2.64) 1.89 0.17
Q4 (≥2.35) 77 6379.75 12.07 2.95 (1.76–4.93) 16.98 <0.001 2.89 (1.72–4.87) 16.02 <0.001
Ptrend <0.001 <0.001 <0.001
Lipid accumulation product
Q1 (<10.11) 22 6448.58 3.41 1 1
Q2 (10.11–20.95) 34 6427.50 5.29 1.45 (0.77–2.73) 1.33 0.25 1.59 (0.84–3.01) 2.03 0.15
Q3 (20.96–40.23) 42 6420.25 6.54 1.98 (1.08–3.62) 4.90 0.03 2.12 (1.15–3.91) 5.75 0.02
Q4 (≥40.24) 89 6386.83 13.93 4.45 (2.57–7.70) 28.46 <0.001 5.02 (2.85–8.85) 31.04 <0.001
Ptrend <0.001 <0.001 <0.001

Model 1 was adjusted for age, family history of diabetes, and a family history of hypertension.
Model 2 was adjusted for the variables in Model 1 as well as education level, marital status, smoking, alcohol consumption, physical activity, and systolic blood pressure.
CI, confidence interval; HDL-C, high-density lipoprotein cholesterol; HR, hazard ratio; Q1–Q4, Quartiles 1–4; TG, triglycerides. *Per 1000 person-years.
Diabetes prevention in China

647
 Table 3 Cox proportional hazards regression analysis of risk of incident type 2 diabetes mellitus by quartiles of fasting plasma glucose, triglycerides: high-density lipoprotein cholesterol ratio,

648
triglyceride glucose index, visceral adiposity index, and lipid accumulation product for men

Model 1 Model 2
2
No. cases No. person-years Incidence* HR (95% CI) χ P-value HR (95% CI) χ2 P-value

Fasting plasma glucose

Q1 (<4.95 mmol/L) 31 10429.50 2.97 1 1
Q2 (4.95–5.25 mmol/L) 38 10217.17 3.72 1.58 (0.92–2.71) 2.70 0.10 1.52 (0.88–2.62) 2.29 0.13
Q3 (5.26–5.55 mmol/L) 57 10040.67 5.68 2.50 (1.51–4.15) 12.58 <0.001 2.35 (1.41–3.90) 10.83 <0.01
Diabetes prevention in China

Q4 (≥5.56 mmol/L) 125 10168.83 12.29 5.50 (3.47–8.70) 52.88 <0.001 5.05 (3.18–8.03) 47.00 <0.001
Ptrend <0.001 <0.001 <0.001
Waist circumference
Q1 (<74.00 cm) 23 9935.58 2.31 1 1
Q2 (74.00–81.04 cm) 44 10467.83 4.20 1.80 (0.99–3.25) 3.74 0.05 1.74 (0.96–3.16) 3.36 0.07
Q3 (81.05–87.99 cm) 60 10074.67 5.96 2.14 (1.19–3.86) 6.46 0.01 1.97 (1.09–3.56) 5.07 0.02
Q4 (≥88.00 cm) 124 10366.08 11.96 4.67 (2.72–7.99) 31.48 <0.001 4.07 (2.36–7.03) 25.49 <0.001
Ptrend <0.001 <0.001 <0.001
TG: HDL-C ratio
Q1 (<0.75) 30 10298.17 2.91 1 1
Q2 (0.75–1.12) 41 10243.17 4.00 1.46 (0.83–2.57) 1.74 0.19 1.39 (0.79–2.45) 1.32 0.25
Q3 (1.13–1.75) 64 10135.75 6.31 2.04 (1.19–3.50) 6.73 <0.01 1.97 (1.15–3.38) 6.05 0.01
Q4 (≥1.76) 111 10082.08 11.01 4.40 (2.68–7.20) 34.48 <0.001 4.05 (2.46–6.67) 30.33 <0.001
Ptrend <0.001 <0.001 <0.001
Triglyceride glucose index
Q1 (<8.27) 21 10441.67 2.01 1 1
Q2 (8.27–8.62) 48 10213.75 4.70 2.55 (1.39–4.68) 9.05 <0.01 2.50 (1.36–4.60) 8.67 <0.01
Q3 (8.63–9.00) 68 10139.25 6.71 3.34 (1.85–6.04) 15.91 <0.001 3.12 (1.72–5.67) 14.00 <0.001
Q4 (≥9.01) 111 10006.58 11.09 6.67 (3.80–11.71) 43.67 <0.001 6.15 (3.48–10.85) 39.25 <0.001
Ptrend <0.001 <0.001 <0.001
Visceral adiposity index
Q1 (<1.36) 27 10285.08 2.63 1 1
Q2 (1.36–2.08) 44 10218.08 4.31 1.82 (1.03–3.23) 4.22 0.04 1.75 (0.99–3.10) 3.64 0.06
Q3 (2.09–3.28) 61 10153.92 6.01 2.25 (1.29–3.94) 8.09 <0.01 2.13 (1.22–3.74) 7.01 0.01
Q4 (≥3.29) 114 10084.08 11.30 4.80 (2.86–8.06) 35.25 <0.001 4.40 (2.61–7.42) 31.00 <0.001
Ptrend <0.001 <0.001 <0.001
Lipid accumulation product
Q1 (<16.74) 17 10275.83 1.65 1 1
Q2 (16.74–30.41) 42 10239.08 4.10 2.48 (1.27–4.86) 7.04 <0.01 2.42 (1.23–4.74) 6.59 0.01
Q3 (30.42–51.83) 69 10166.92 6.79 3.96 (2.10–7.49) 18.01 <0.001 3.65 (1.92–6.92) 15.69 <0.001
Q4 (≥51.84) 120 10107.42 11.87 7.26 (3.92–13.43) 39.80 <0.001 6.49 (3.48–12.12) 34.57 <0.001
Ptrend <0.001 <0.001 <0.001

Model 1 was adjusted for age, family history of diabetes, and a family history of hypertension.
Model 2 was adjusted for the variables in Model 1 as well as education level, marital status, smoking, alcohol consumption, physical activity, and systolic blood pressure.
CI, confidence interval; HDL-C, high-density lipoprotein cholesterol; HR, hazard ratio; Q1–Q4, Quartiles 1–4; TG, triglycerides. *Per 1000 person-years.
B. WANG et al.

© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
B. WANG et al. Diabetes prevention in China

Figure 2 Receiver operating characteristic (ROC) curves in (a) men and (b) women for fasting plasma glucose (FPG), waist circumference
(WC), triglyceride (TG) to high-density lipoprotein cholesterol (HDL-C) ratio, triglyceride glucose index (TyG), visceral adiposity index (VAI), and
the lipid accumulation product (LAP) for predicting type 2 diabetes mellitus.

However, compared with other routine biomarkers, the
ability of TyG to identify T2DM is controversial in dif-
ferent ethnic groups. In a European population, TyG
was a better predictor of T2DM development in normo-
glycemic people than either FPG or TG.15 In an
Iranian population, TyG did not improve diabetes pre-
diction compared with FPG, 1-h plasma glucose, or 2-h
plasma glucose.14 In the present study, the risk of inci-
dent T2DM was increased with elevated TyG values in
both men and women. For predicting T2DM risk, the
AUCs for TyG did not differ from those for individual
measures (FPG and WC) for either men or women
among rural Chinese people.
Adipose tissue is generally considered to play a cen-
tral role in lipid and glucose metabolism.40 Excessive
visceral adipose tissue accumulation is closely associ-
ated with the risk of incident cardiovascular diseases
and T2DM.4,41 The VAI includes body physical and
metabolic factors and may indirectly reflect cardiometa-
bolic risk factors, including altered production of adipo-
cytokines, increased lipolysis, and increased plasma free
fatty acid content.10 Previous studies showed that VAI
was significantly associated with T2DM and more effi-
cient than the TG: HDL-C ratio, but not superior to
BMI, WC, or waist-to-height ratio, in detecting T2DM
among non-T2DM people.12,16,18 Consistent with

Table 4 Receiver operating characteristic analysis for fasting plasma glucose, waist circumference, triglycerides: high-density lipoprotein cho-
lesterol ratio, triglyceride glucose index, visceral adiposity index, and lipid accumulation product for predicting type 2 diabetes mellitus at the
6-year follow-up in men and women separately

Cut-off value AUC (95% CI) Sensitivity (%) Specificity (%) PPV (%) NPV (%)
Men
FPG (mmol/L) 5.6 0.638 (0.623–0.652) 42.55 80.30 9.05 96.81
WC (cm) 87.45 0.654 (0.640–0.669) 58.51 69.75 8.18 97.33
TG: HDL-C ratio 1.69 0.613 (0.598–0.628) 47.59 71.93 7.23 96.76
TyG 8.72 0.625 (0.610–0.639) 59.89 60.75 6.55 97.06
VAI 2.25 0.622 (0.607–0.636) 47.06 74.23 7.75 96.82
LAP 36.96 0.653 (0.638–0.667) 51.34 73.02 8.04 97.03
Women
FPG (mmol/L) 5.44 0.664 (0.652–0.675) 60.56 66.77 6.49 97.80
WC (cm) 82.05 0.669 (0.657–0.680) 70.92 55.00 5.66 98.03
TG: HDL-C ratio 1.17 0.644 (0.632–0.655) 69.92 52.90 5.26 97.92
TyG 8.79 0.669 (0.657–0.680) 62.90 62.62 5.96 97.82
VAI 2.50 0.654 (0.642–0.665) 63.41 61.41 5.79 97.82
LAP 37.84 0.693 (0.682–0.704) 69.35 61.49 6.35 98.16

AUC, area under the receiver operating characteristic curve; CI, confidence interval; FPG, fasting plasma glucose; HDL-C, high-density lipopro-
tein cholesterol; LAP, lipid accumulation product; NPV, negative predictive value; PPV, positive predictive value; TG, triglycerides; TyG, triglyc-
eride glucose index; VAI, visceral adiposity index; WC, waist circumference.

© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd 649
Diabetes prevention in China
previous studies, the present study revealed larger
AUCs for VAI than the TG: HDL-C ratio for detect-
ing T2DM in both sexes. The VAI was equivalent to
FPG and WC for detecting T2DM in both men and
women.
The LAP has been reported as a reliable visceral adi-
posity index combining TG levels and WC for predict-
ing IR, T2DM, and cardiovascular diseases.12,26 The
phenotype of a hypertriglyceridemic waist (large waist
with elevated TG levels) could be an inexpensive screen-
ing tool to predict the atherogenic metabolic triad
(hyperinsulinemia, elevated apolipoprotein B levels, and
small, dense LDL-C particles) for men.42 A meta-
analysis has also suggested that the risk of T2DM is
closely associated with the hypertriglyceridemic waist
phenotype in the general population.43 Alternatively, as
a continuous index, LAP has been developed to reflect
the combined anatomic and physiologic changes associ-
ated with overaccumulation of lipids in adults.26 In the
present study, we found that the risk of incident T2DM
was associated with elevated LAP in both sexes. Com-
pared with FPG, LAP had a higher sensitivity but
lower specificity for predicting T2DM risk in both
sexes. Compared with WC, LAP had a lower sensitivity
and higher specificity for predicting T2DM risk in men
and a similar sensitivity but higher specificity in women.
The AUCs for LAP did not differ from those for FPG
and WC in men and women.
The present study was a well-designed and
population-based prospective cohort study with a low
rate of loss to follow-up and standardized anthropomet-
ric, physical, and laboratory measurements to compare
the association of traditional individual measures, lipid
ratios, and three novel indices (TyG, VAI, LAP) with
the risk of incident T2DM in a rural Chinese popula-
tion. However, the present study has some limitations.
We did not use a 2-h oral glucose tolerance test or mea-
sure HbA1c levels to diagnose T2DM, so we may have
underestimated the incidence of T2DM, and this may
affect the association between different indicators and
T2DM. In addition, the participants in the present
study were from a rural population in the middle of
China, which may not represent the characteristics of
other Chinese people well.
In conclusion, elevated TyG, VAI, and LAP are sig-
nificantly associated with the risk of incident T2DM in
both men and women in rural China. For discriminat-
ing T2DM, TyG, VAI, and LAP were mostly superior
to the TG: HDL-C ratio and equal to FPG and WC
for predicting T2DM at follow-up. According to eco-
nomic benefits, as compound indices, TyG, VAI, and
LAP did not improve T2DM prediction compared with
measurement of FPG or WC alone. Therefore, TyG,
650 © 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
B. WANG et al.
VAI, and LAP may not be a convenient or inexpensive
approach for predicting T2DM in rural Chinese people.
Acknowledgements
This study was supported by the National Natural Sci-
ence Foundation of China (Grant no. 81373074,
81402752, and 81673260) and the Science and Technol-
ogy Development Foundation of Shenzhen (Grant no.
JCYJ20140418091413562, JCYJ 20160307155707264,
JCYJ 20170302143855721, and JCYJ 20170412110537191).
Disclosure
None declared.
References
1. International Diabetes Federation (IDF). IDF Diabetes
Atlas – 7th Edition. 2015. Brussels, Belgium: International
Diabetes Federation. Available from: http://www.
diabetesatlas.org/key-messages.html (accessed 17 February
2017).
2. Xu Y, Wang L, He J et al. Prevalence and control of
diabetes in Chinese adults. JAMA. 2013; 310: 948–59.
3. Wang L, Wang A, Zhou D, FitzGerald G, Ye D,
Jiang Q. An empirical analysis of rural–urban differ-
ences in out-of-pocket health expenditures in a low-
income society of China. PLoS One. 2016; 11:
e0154563.
4. Liu PJ, Ma F, Lou HP, Chen Y. Visceral adiposity index
is associated with pre-diabetes and type 2 diabetes melli-
tus in Chinese adults aged 20–50. Ann Nutr Metab. 2016;
68: 235–43.
5. Dugani SB, Akinkuolie AO, Paynter N, Glynn RJ,
Ridker PM, Mora S. Association of lipoproteins, insulin
resistance, and rosuvastatin with incident type 2 diabetes
mellitus: Secondary analysis of a randomized clinical
trial. JAMA Cardiol. 2016; 1: 136–45.
6. McLaughlin T, Lamendola C, Liu A, Abbasi F. Prefer-
ential fat deposition in subcutaneous versus visceral
depots is associated with insulin sensitivity. J Clin Endo-
crinol Metab. 2011; 96: E1756–60.
7. Vasques AC, Novaes FS, de Oliveira Mda S et al. TyG
index performs better than HOMA in a Brazilian popu-
lation: A hyperglycemic clamp validated study. Diabetes
Res Clin Pract. 2011; 93: e98–e100.
8. Cheung AS, de Rooy C, Hoermann R et al. Correlation
of visceral adipose tissue measured by lunar prodigy dual
X-ray absorptiometry with MRI and CT in older men.
Int J Obesity. 2016; 40: 1325–8.
9. Guerrero-Romero F, Simental-Mendia LE, Gonzalez-
Ortiz M et al. The product of triglycerides and glucose, a
simple measure of insulin sensitivity. Comparison with
the euglycemic–hyperinsulinemic clamp. J Clin Endocri-
nol Metab. 2010; 95: 3347–51.
B. WANG et al.
10. Amato MC, Giordano C, Galia M et al. Visceral adipos-
ity index: A reliable indicator of visceral fat function
associated with cardiometabolic risk. Diabetes Care.
2010; 33: 920–2.
11. Du T, Yuan G, Zhang M, Zhou X, Sun X, Yu X. Clini-
cal usefulness of lipid ratios, visceral adiposity indicators,
and the triglycerides and glucose index as risk markers of
insulin resistance. Cardiovasc Diabetol. 2014; 13: 146.
12. Er LK, Wu S, Chou HH et al. Triglyceride glucose–body
mass index is a simple and clinically useful surrogate
marker for insulin resistance in nondiabetic individuals.
PLoS One. 2016; 11: e0149731.
13. Amato MC, Magistro A, Gambino G, Vesco R,
Giordano C. Visceral adiposity index and DHEAS are
useful markers of diabetes risk in women with polycystic
ovary syndrome. Eur J Endocrinol. 2015; 172: 79–88.
14. Janghorbani M, Almasi SZ, Amini M. The product of
triglycerides and glucose in comparison with fasting
plasma glucose did not improve diabetes prediction. Acta
Diabetol. 2015; 52: 781–8.
15. Navarro-Gonzalez D, Sanchez-Inigo L, Pastrana-
Delgado J, Fernandez-Montero A, Martinez JA. Triglycer-
ide–glucose index (TyG index) in comparison with fasting
plasma glucose improved diabetes prediction in patients
with normal fasting glucose: The vascular-metabolic CUN
cohort. Prev Med. 2016; 86: 99–105.
16. Janghorbani M, Amini M. The visceral adiposity index
in comparison with easily measurable anthropometric
markers did not improve prediction of diabetes. Can J
Diabetes. 2016; 40: 393–8.
17. Wakabayashi I, Daimon T. A strong association
between lipid accumulation product and diabetes melli-
tus in japanese women and men. J Atheroscler Thromb.
2014; 21: 282–8.
18. Zhang M, Zheng L, Li P et al. 4-Year trajectory of vis-
ceral adiposity index in the development of type 2 diabe-
tes: A prospective cohort study. Ann Nutr Metab. 2016;
69: 142–9.
19. Li YQ, Sun CQ, Li LL et al. Resting heart rate as a
marker for identifying the risk of undiagnosed type 2 dia-
betes mellitus: A cross-sectional survey. BMC Public
Health. 2014; 14: 1052.
20. Zhang M, Wang B, Liu Y et al. Cumulative increased
risk of incident type 2 diabetes mellitus with increasing
triglyceride glucose index in normal-weight people: The
rural Chinese cohort study. Cardiovasc Diabetol. 2017;
16: 30.
21. Zhao Y, Zhang M, Luo X et al. Association of obesity
categories and high blood pressure in a rural adult Chi-
nese population. J Hum Hypertens. 2016; 30: 613–8.
22. American Diabetes Association. Standards of medical
care in diabetes. Diabetes Care. 2005; 28 (Suppl. 1):
S4–36.
23. Van Holle V, De Bourdeaudhuij I, Deforche B, Van
Cauwenberg J, Van Dyck D. Assessment of physical
activity in older Belgian adults: Validity and reliability of
an adapted interview version of the long International
Physical Activity Questionnaire (IPAQ-L). BMC Public
Health. 2015; 15: 433.
© 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd
Diabetes prevention in China
24. Perloff D, Grim C, Flack J et al. Human blood pressure
determination by sphygmomanometry. Circulation. 1993;
88: 2460–70.
25. Bairaktari E, Hatzidimou K, Tzallas C et al. Estimation
of LDL cholesterol based on the Friedewald formula
and on apo B levels. Clin Biochem. 2000; 33: 549–55.
26. Kahn HS. The “lipid accumulation product” performs
better than the body mass index for recognizing cardio-
vascular risk: A population-based comparison. BMC
Cardiovasc Disord. 2005; 5: 26.
27. DeLong ER, DeLong DM, Clarke-Pearson DL. Com-
paring the areas under two or more correlated receiver
operating characteristic curves: A nonparametric
approach. Biometrics. 1988; 44: 837–45.
28. Song Q, Liu X, Wang A et al. Associations between
non-traditional lipid measures and risk for type 2 diabetes
mellitus in a Chinese community population: A cross-
sectional study. Lipids Health Dis. 2016; 15: 70.
29. Lin D, Qi Y, Huang C et al. Associations of lipid param-
eters with insulin resistance and diabetes: A population-
based study. Clin Nutrition. 2017. https://doi.org/10.1016/
j.clnu.2017.06.018.
30. Giannini C, Santoro N, Caprio S et al. The triglyceride-
to-HDL cholesterol ratio: Association with insulin resis-
tance in obese youths of different ethnic backgrounds.
Diabetes Care. 2011; 34: 1869–74.
31. Gao H, Salim A, Lee J, Tai ES, van Dam RM. Can
body fat distribution, adiponectin levels and inflamma-
tion explain differences in insulin resistance between eth-
nic Chinese, Malays and Asian Indians? Int J Obesity.
2012; 36: 1086–93.
32. Janghorbani M, Amini M. Utility of serum lipid ratios
for predicting incident type 2 diabetes: The Isfahan dia-
betes prevention study. Diabetes Metab Res Rev. 2016;
32: 572–80.
33. Hadaegh F, Hatami M, Tohidi M, Sarbakhsh P,
Saadat N, Azizi F. Lipid ratios and appropriate cut off
values for prediction of diabetes: A cohort of Iranian
men and women. Lipids Health Dis. 2010; 9: 85.
34. McPhillips JB, Barrett-Connor E, Wingard DL. Cardio-
vascular disease risk factors prior to the diagnosis of
impaired glucose tolerance and non-insulin-dependent
diabetes mellitus in a community of older adults.
Am J Epidemiol. 1990; 131: 443–53.
35. Tirosh A, Shai I, Bitzur R et al. Changes in triglyceride
levels over time and risk of type 2 diabetes in young
men. Diabetes Care. 2008; 31: 2032–7.
36. Lillioja S, Mott DM, Spraul M et al. Insulin resistance
and insulin secretory dysfunction as precursors of non-
insulin-dependent diabetes mellitus. Prospective studies
of Pima Indians. N Engl J Med. 1993; 329: 1988–92.
37. Lupi R, Del Guerra S, Fierabracci V et al. Lipotoxicity
in human pancreatic islets and the protective effect of
metformin. Diabetes. 2002; 51 (Suppl. 1): S134–7.
38. Unger RH. Lipotoxicity in the pathogenesis of obesity-
dependent NIDDM. Genetic and clinical implications.
Diabetes. 1995; 44: 863–70.
39. Robertson RP, Harmon J, Tran PO, Poitout V. Beta-cell
glucose toxicity, lipotoxicity, and chronic oxidative stress
651
Diabetes prevention in China B. WANG et al.

in type 2 diabetes. Diabetes. 2004; 53 (Suppl. 1): 42. Lemieux I, Pascot A, Couillard C
S119–24. et al. Hypertriglyceridemic waist: A marker of the ath-
40. Hajer GR, van Haeften TW, Visseren FL. Adipose tissue erogenic metabolic triad (hyperinsulinemia; hyperapoli-
dysfunction in obesity, diabetes, and vascular diseases. poprotein B; small, dense LDL) in men? Circulation.
Eur Heart J. 2008; 29: 2959–71. 2000; 102: 179–84.
41. Yusuf S, Hawken S, Ounpuu S et al. Obesity and the risk 43. Ren Y, Luo X, Wang C et al. Prevalence of hypertrigly-
of myocardial infarction in 27,000 participants from ceridemic waist and association with risk of type 2 diabe-
52 countries: A case-control study. Lancet. 2005; 366: tes mellitus: A meta-analysis. Diabetes Metab Res Rev.
1640–9. 2016; 32: 405–12.

652 © 2018 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd