Received: 17 February 2020 | Revised: 12 March 2020 | Accepted: 16 March 2020

DOI: 10.1111/jch.13878

ORIG INAL PAPER

Association of triglyceride glucose index and its combination

of obesity indices with prehypertension in lean individuals: A
cross-sectional study of Chinese adults

Zhen Yu Zeng MD1 | Su Xuan Liu MD1 | Hao Xu MD2 | Xia Xu MD3 |
Xing Zhen Liu MD4 | Xian Xian Zhao MD1

1
Department of Cardiology, Changhai
Hospital, Naval Military Medical University Abstract
(The Second Military Medical University), For normal-weight population, the management of prehypertension may be more
Shanghai, China
2 beneficial by identifying insulin resistance (IR) status than relying solely on traditional
Department of Infectious Diseases,
Changhai Hospital, Naval Military Medical indicators of obesity. We investigated the association of triglyceride glucose (TyG)
University (The Second Military Medical
index, a simple surrogate marker of IR, and its combination of obesity indices with
University), Shanghai, China
3
Department of Rheumatology, Changhai
prehypertension in lean individuals. A total of 105 070 lean adults without hyper-
Hospital, Naval Military Medical University tension were included in this analysis. Body mass index (BMI), waist circumference
(The Second Military Medical University),
Shanghai, China
(WC), waist-to-height ratio (WtHR), and TyG were calculated according to the corre-
4
Hangzhou Aeronautical Sanatorium of sponding formula; TyG-BMI, TyG-WC, and TyG-WHtR were calculated by multiply-
Chinese Air Force, Hangzhou, China ing the corresponding two parameters. Gardner-Altman plots, partial correlation, and
Correspondence logistic regression analyses were applied to explore the associations in continuous
Xian Xian Zhao, Department of Cardiology, variables and quartiles. The prehypertensive ones had higher mean values of TyG,
Changhai Hospital, Naval Military Medical
University, No. 168, Changhai Road, Yangpu TyG-BMI, TyG-WC, and TyG-WHtR than normotensive individuals. All the four indi-
District, Shanghai, 200433, China. cators showed positive correlations with systolic blood pressure and diastolic blood
Email: 13601713431@163.com
pressure. After full adjustment, only TyG-BMI and TyG-WC were significantly associ-
Xing Zhen Liu, Hangzhou Aeronautical
Sanatorium of Chinese Air Force, No. 27,
ated with prehypertension in both genders. Furthermore, TyG-BMI had the highest
Yang Gong Di, Xihu District, Hangzhou, OR for prehypertension. Our study showed that TyG-BMI might be an accessible and
Zhejiang, 310007 China.
Email: xzliu7@163.com
complementary monitor in the hierarchical management of non-obese prehyperten-
sive patients.
Funding information
This work was supported by National
Natural Science Foundation of China
(81570208).

1 | I NTRO D U C TI O N the 2017 ACC/AHA Hypertension Guideline defined 130-139/80-

Hypertension is a worldwide healthy problem and well-known fac-
tor for cardiovascular disease (CVD).1 Recent two decades, although
within the normal range, a slightly elevated blood pressure (BP)
also attracted much attention due to its unfavorable clinical impli-
2-4
cation. So the JNC-7 announced prehypertension (120-139/80-
89 mmHg) as a new BP classification criteria in 2003.5 In 2017,
89 mmHg as stage 1 hypertension.6
Although elevated BP is often accompanied by obesity which
is often assessed by body mass index (BMI), many individuals with
normal BMI are also characterized by elevated BP, especially in East
Asian populations.7 So if some people are prehypertensive and have
normal weight, they generally tend to ignore their BP issues, and
the primary health care provider also does not know how to manage

Zhen Yu Zeng, Su Xuan Liu, Hao Xu contributed equally to this work.

J Clin Hypertens. 2020;22:1025–1032. wileyonlinelibrary.com/journal/jch© 2020 Wiley Periodicals LLC | 1025

 |
1026
them.8 Considering that insulin resistance (IR) is a vital pathologi-
9
cal mechanism of elevated BP, recognition of IR in lean prehyper-
tensive individuals may be of substantial clinical importance for the
management of prehypertension.
More recently, triglyceride glucose (TyG) index, the product
of fasting plasma glucose (FPG), and triglycerides (TG) have been
proposed as simple and efficient surrogate marker for early identi-
fication of IR.10 In addition, TyG combined with BMI, waist circum-
ference (WC), and waist-to-height ratio (WtHR) have been reported
11
they are more efficient than TyG alone. But no studies have yet
been conducted regarding the relationship between these param-
eters and prehypertension in individuals with normal weight. Thus,
this large-scale cross-sectional study was designed to investigate
the associations of TyG, TyG-BMI, TyG-WC, and TyG-WHtR with
prehypertension in lean Chinese adults.
2 | M E TH O DS
2.1 | Subjects
This study was based on the database of adults who received rou-
tine physical examination between January 2013 and July 2019 in
the Yangtze River Delta of China. (reviewer #1, comment #2) These
people who received routine physical examination were “apparently
healthy” and without specific complaints or severe disease, which
mean they were either healthy or only suffered from some common
chronic diseases such as hypertension, diabetes, fatty liver, dyslipi-
demia, or hyperuricemia, and thyroid nodules. (reviewer #2, com-
ment #3) (reviewer #2, comment #4).
Considering the calculation of TyG needs FPG and TG, so those
who took hypoglycemic agents and lipid-lowering drugs were ex-
cluded. This study focused on patients with prehypertension, so
those with hypertension (140/90 mmHg, or self-report history of hy-
pertension, or current use of antihypertensive medication) were also
excluded. Finally, a total of 105 070 lean adults (with BMI 18-24 kg/
m2) without hypertension were analyzed in this study. The study
was approved by the ethics committee of Hangzhou Aeronautical
Sanatorium of Chinese Air Force.
2.2 | Data collection
Anthropometric indicators were measured by well-trained examiners
and in light clothing with no shoes. The systolic blood pressure (SBP),
diastolic blood pressure (DBP), and heart rate (HR) were obtained
three times on the right arm after at least 5-minute rest using auto-
matic BP monitor (HEM-1000, OMRON, Japan). The blood samples of
subjects were collected after a minimum of 8 hour of overnight fasting.
Serum levels of FPG, plasma uric acid (UA), total cholesterol (TC), TG,
low-density lipoprotein cholesterol (LDLc), high-density lipoprotein
cholesterol (HDLc), alanine aminotransferase (ALT), aspartate ami-
notransferase (AST), alkaline phosphatase (ALP), and gamma-glutamyl
17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ZENG et al.
transferase (GGT) were determined by a biochemical autoanalyzer
(Advia 1650 Autoanalyzer; Bayer Diagnostics). Abdominal ultrasonog-
raphy (ATL HDI 5000; Phillips Medical Systems) was undertaken by
clinical radiologists using a 3.5 MHz probe for all subjects.
2.3 | Definitions
Prehypertension was defined as having either a SBP of 120-
139 mmHg and/or DBP of 80-89 mmHg. (reviewer #1, comment #8)
BMI was calculated as weight divided by the square of height; WC di-
vided by the hip circumference (reviewer #1, comment #9) was WHR;
WC divided by height provided the WHtR. TyG = Ln [fasting TG (mg/
dL)*FPG (mg/dL)/2]9; TyG-BMI = TyG × BMI; TyG-WC = TyG × WC;
TyG-WHtR = TyG × WHtR.
2.4 | Statistical analysis
Statistical analysis was performed using SPSS version 18.0 (SPSS Inc)
and MedCalc version 19.0 (MedCalc Software). (reviewer #1, com-
ment #10) (reviewer #2, comment #6) Data are expressed as numbers
or means ± SD. Categorical variables were compared using the chi-
squared test, and t test was used to test the differences in continuous
data. Gardner-Altman plots were produced using estimation statistics
for data visualization. Partial correlation was applied to examine the
correlation between BP levels and TyG and its related parameters,
which was adjusted for age, biochemical indicators, alcohol intake,
smoking status, and non-alcoholic fatty liver disease.(reviewer #1,
comment #2) Logistic regression analyses were applied to explore
the associations of TyG and its related parameters with prehyperten-
sion. TyG, TyG-BMI, TyG-WC, and TyG-WHtR were divided into four
quartiles, and the lowest quartile was used as a reference in regres-
sion analysis. Adjustment conditions were the same as partial corre-
lation analysis. Receiver operating characteristic (ROC) analyses and
the area under ROC curves (AUC) were used to evaluate the ability
of these indicators to distinguish prehypertension. AUCs of different
indicators were compared by DeLong method in MedCalc. (reviewer
#2, comment #6) P-value < .05 was considered statistically significant.
3 | R E S U LT S
The mean age of 105 070 lean adults without hypertension was
42.6 years and 54.7% were women. The overall proportion of prehy-
pertension was 39.7%, (reviewer #1, comment #4) and 29.5% in lean
women and 52.1% in lean men. The clinical characteristics of lean in-
dividuals without hypertension are shown in Table 1. Compared to
normotensive individuals, the prehypertensive ones were older, slight
fatter, with a higher levels of HR and liver enzymes, and less favorable
metabolic profile. (reviewer #1, comment #11) (reviewer #1, comment
#13) In addition, prehypertensive ones had higher mean values of
TyG, TyG-BMI, TyG-WC, and TyG-WHtR in both genders (Figure 1).
 |

17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ZENG et al. 1027

TA B L E 1 The clinical characteristics of lean individuals without hypertension

Women Men

Characteristics Normotension Prehypertension P value Normotension Prehypertension P value

No., n 40 500 16 968 - 22 818 24 784 -

Age, y 39.5 ± 10.2 45.3 ± 13.0 <.001 40.5 ± 11.6 42.0 ± 13.5 <.001
BMI (kg/m2) 20.7 ± 1.8 21.3 ± 1.8 <.001 21.5 ± 1.8 21.9 ± 1.6 <.001
WC (cm) 68.9 ± 5.6 70.8 ± 5.9 <.001 76.2 ± 6.0 77.3 ± 5.9 <.001
WHR 0.77 ± 0.05 0.79 ± 0.06 <.001 0.83 ± 0.05 0.84 ± 0.05 <.001
WHtR 0.43 ± 0.04 0.44 ± 0.04 <.001 0.44 ± 0.04 0.45 ± 0.03 <.001
SBP (mmHg) 105.9 ± 8.2 126.1 ± 6.4 <.001 109.4 ± 7.1 126.9 ± 6.3 <.001
DBP (mm Hg) 65.0 ± 6.9 75.8 ± 7.5 <.001 68.0 ± 6.2 77.6 ± 6.7 <.001
Heart rate (beats/min) 81.0 ± 11.4 84.5 ± 13.7 <.001 76.2 ± 11.6 80.4 ± 12.9 <.001
FPG (mmol/L) 5.28 ± 0.54 5.50 ± 0.80 <.001 5.45 ± 0.86 5.62 ± 1.02 <.001
TC (mmol/L) 4.56 ± 0.84 4.82 ± 0.91 <.001 4.58 ± 0.83 4.68 ± 0.86 <.001
TG (mmol/L) 0.96 ± 0.58 1.13 ± 0.73 <.001 1.29 ± 0.89 1.41 ± 1.03 <.001
HDLc (mmol/L) 1.71 ± 0.34 1.71 ± 0.36 .655 1.47 ± 0.31 1.48 ± 0.32 <.001
LDLc (mmol/L) 2.36 ± 0.69 2.56 ± 0.75 <.001 2.51 ± 0.70 2.57 ± 0.72 <.001
UA (μmol/L) 263.0 ± 52.3 269.5 ± 56.3 <.001 362.1 ± 68.4 365.3 ± 70.9 <.001
ALT (U/L) 17.3 ± 12.2 18.7 ± 17.8 <.001 24.6 ± 18.6 26.1 ± 24.1 <.001
AST (U/L) 18.5 ± 7.3 19.4 ± 9.5 <.001 21.0 ± 10.8 21.7 ± 11.7 <.001
ALP (U/L) 56.4 ± 16.2 61.7 ± 18.5 <.001 67.1 ± 17.3 68.3 ± 17.1 <.001
GGT (U/L) 17.0 ± 14.0 19.2 ± 17.1 <.001 29.5 ± 29.3 34.0 ± 36.5 <.001

Abbreviations: ALP, alkaline phosphatase; ALT, alanine aminotransferase; AST, aspartate aminotransferase; BMI, body mass index; DBP, diastolic
blood pressure; FPG, fasting plasma glucose; GGT, gamma-glutamyl transpeptidase. HDLc, high-density lipoprotein cholesterol; LDLc, low-density
lipoprotein cholesterol; SBP, systolic blood pressure; TC, total cholesterol; TG, triglyceride; UA, plasma uric acid; WC, waist circumference; WHR,
waist-to-hip ratio; WHtR, waist-to-height ratio.

After controlling for confounding factors, TyG, TyG-BMI,
TyG-WC, and TyG-WHtR were significantly correlated with each
other (Table S1) and BP levels in both genders (Table 2). (reviewer
#1, comment #7) The SBP and DBP levels were significantly elevated
from the lowest to top quartiles of TyG, TyG-BMI, TyG-WC, and
TyG-WHtR. Similarly, the proportion of prehypertension showed a
significant increase trend as ascending quartiles of TyG, TyG-BMI,
TyG-WC, and TyG-WHtR in both genders (Table 3).
Results of logistic regression analysis are shown in Figure 2.
After full adjustment, TyG-BMI and TyG-WC were significantly as-
sociated with prehypertension in both genders, whereas TyG was
significantly associated with prehypertension only in women and
TyG-WHtR was not significantly associated with prehypertension in
both genders. In women, the OR for prehypertension in the highest
quartile of TyG, TyG-BMI, TyG-WC were 1.299 (95% CI 1.185-1.423),
1.628 (95% CI 1.455-1.821), and 1.379 (95% CI 1.180-1.611), respec-
tively; In men, the OR for prehypertension in the highest quartile of
TyG-BMI and TyG-WC were 1.669 (95% CI 1.482-1.881), 1.355 (95%
CI 1.169-1.571), respectively.
The ROC curves of traditional obesity indicators, (reviewer #2,
comment #2) TyG, and its related parameters for prehypertension are
shown in Figure S1. The AUC value of TyG, TyG-BMI, TyG-WC, and
TyG-WHtR to distinguish prehypertension are summarized in Table 4.
Among women, no significant difference in the AUC of TyG-BMI
[0.619 (95% CI 0.614-0.625)], TyG-WC [0.618 (95% CI 0.612-0.623)],
and TyG-WHtR [0.619 (95% CI 0.613-0.624)], which were signifi-
cantly higher than that of TyG [0.605 (95% CI 0.600-0.611)]. Among
men, TyG-BMI had the largest AUC for prehypertension [0.570 (95%
CI 0.564-0.575)]. The results of pairwise comparisons between indi-
cators are shown in Table S2. (reviewer #2, comment #6).
4 | D I S CU S S I O N
In this large-scale cross-sectional study, we investigated the associa-
tion of TyG and its combination of obesity indices with prehyper-
tension in lean Chinese adults. Our data revealed that, although in
normal-weight individuals, the combination of adiposity status and
TyG (TyG-BMI and TyG-WC) still showed a strong and positive as-
sociation with prehypertension in both genders. Moreover, TyG-BMI
outperformed other parameters with a higher OR and larger AUC.
The results suggested that TyG-BMI might be an accessible and ef-
fective assessment indicator in the hierarchical management of lean
prehypertensive individuals.
Elevated BP is the most common comorbidity of obesity.12
Nevertheless, there is also a certain proportion of prehyperten-
sion in individuals with normal BMI, especially in Asian popula-
tions.13 Most studies on elevated BP in lean people have focused
 |
1028
on populations in low- to middle-income countries.14 In the present
study, unlike previous research, our research subjects are the pop-
ulation in the Yangtze River Delta region, where is one of the most
developed regions in China. This study may provide some informa-
tion for the prevention and treatment of hypertension in lean popu-
lations in high- and middle-income areas. (reviewer #1, comment #2).
Prehypertension is a common condition that affects 25%-50% of
15
adults worldwide. In this study, the overall proportion of prehyper-
tension among the lean subjects was 39.7% which was higher than the
reported proportion of China and other East Asian populations that
were not grouped by BMI (31%-37%).16,17 The main reason was that we
excluded hypertensive and overweight/obese individuals which made
the base of the study population less. (reviewer #1, comment #4).
Another interesting result of this study was that the proportion
of prehypertension in lean men was significantly higher than that
17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ZENG et al.
F I G U R E 1 Gardner-Altman plots for
TyG, TyG-BMI, TyG-WC, and TyG-WHtR
according blood pressure status. The raw
data of TyG and its related parameters
were shown on the left axis, and the mean
difference between the two groups was
depicted as a red dotted line and was
shown on the right; BMI, body mass index;
TyG, triglyceride and glucose index; WC,
waist circumference; WHtR, waist-to-
height ratio
in lean women (52.1% vs 29.5%). Beyond the disparity in gender it-
self, another possible explanation for this relatively large difference
may be the source of the study population. In China, the routine
physical examination is not covered by government health insur-
ance, and individuals need to pay for physical examinations them-
selves. However, many enterprises and institutions organize routine
physical examinations for their employees every year, which is an
employee benefit. So most of the subjects in this study were occupa-
tional population. Our previous study suggested that these men had
worse metabolic conditions, which may be related to their occupa-
tional stress and unhealthy lifestyles.18 (reviewer #1, comment #4).
For the management of prehypertension, weight management
based on dietary and exercise interventions intervention is still
the most important method,19 even in normal-weight population.
Several studies and meta-analysis have demonstrated that the risk
 |

17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ZENG et al. 1029

of hypertension associated with adiposity is greater in lean than in In this study, the lean prehypertensive ones were indeed slight fat-
14,20
not-lean subjects. Being as lean as possible within the normal ter than lean normotensive individuals. However, the difference be-
BMI range may be the best suggestion to prevent hypertension. 21,22 tween these traditional obesity indicators was too small to grasp in
clinical practice. So some alternative clinical indicators are needed
to help stratify the lean prehypertensive individuals and play a mon-
TA B L E 2 Partial correlations coefficients between blood
itoring role in the management.
pressure level and TyG and its related parameters
Given that IR is the core pathological mechanism of chronic
SBP DBP metabolic disease,9 identification of IR may help to stratify lean in-
dividuals with prehypertension and develop targeted management
P P
Variable r values r values strategies. Nevertheless, estimating IR remains a challenge in clini-
cal practice. The hyperinsulinemic-euglycemic clamp (HEC), the gold
TyG
standard for assessing IR, is a time- and resource-consuming tool
Women 0.121 <.001 0.128 <.001
and unsuitable for routine clinical practice. 23 Although homeostasis
Men 0.068 <.001 0.135 <.001
model assessment of IR (HOMA-IR) has a wide range of clinical ap-
TyG-BMI
plications, the relative high cost and low repeatability of measuring
Women 0.144 <.001 0.122 <.001
plasma insulin also limits the application of HOMA-IR. 24 In clinical
Men 0.115 <.001 0.150 <.001 work, the accuracy of insulin measurement is easily affected by the
TyG-WC choice of kits, calibration set-up in kits, and conversions between
Women 0.141 <.001 0.116 <.001 units. One study showed that the value of HOMA2-IR calculated by
Men 0.100 <.001 0.141 <.001 11 insulin kits varied by up to twofold. 25 (reviewer #1, comment #6).
TyG-WHtR Unlike HEC and HOMA-IR, TyG does not require insulin but
Women 0.147 <.001 0.111 <.001 only FPG and TG (the two most commonly used clinical indicators),

Men 0.106 <.001 0.141
Note: All adjusted for age, biochemical indicators, alcohol intake,
smoking status, and non-alcoholic fatty liver disease.
Abbreviations: BMI, body mass index; DBP, diastolic blood pressure;
SBP, systolic blood pressure; TyG, triglyceride and glucose index; WC,
waist circumference; WHtR, waist-to-height ratio.
<.001 which not only reduces costs but also improves the stability of the
IR evaluation.26,27 (reviewer #1, comment #6) Subsequent studies
confirmed that TyG closely related to type 2 diabetes, prehyper-
tension, hypertension, hyperuricemia, and CVD.28 Nevertheless,
the research on TyG in lean populations is relatively rare. A recent
study showed that TyG was associated with carotid atherosclerosis

TA B L E 3 The change of blood pressure level and the proportion of prehypertension by quartiles of TyG and its related parameters

Women Men

Variable Q1 Q2 Q3 Q4 Q1 Q2 Q3 Q4

TyG

SBP (mmHg) 110.6 ± 12.9 112.4 ± 13.9 115.0 ± 15.3 121.0 ± 17.8 120.8 ± 14.5 121.7 ± 15.0 123.3 ± 15.3 126.2 ± 16.3

DBP (mm Hg) 67.3 ± 9.2 68.6 ± 9.5 70.0 ± 10.0 72.7 ± 10.7 73.2 ± 9.8 74.5 ± 9.9 76.2 ± 10.2 78.7 ± 10.6

Prehypertension (%) 21.7 25.4 30.8 41.8 47.0 48.8 53.2 57.6

TyG-BMI

SBP (mmHg) 109.8 ± 13.0 112.2 ± 13.8 115.5 ± 15.3 121.5 ± 17.3 119.3 ± 14.6 122.3 ± 15.1 123.6 ± 15.1 126.7 ± 16.0

DBP (mm Hg) 67.4 ± 9.1 68.4 ± 9.5 69.9 ± 10.1 72.9 ± 10.7 72.7 ± 9.5 74.7 ± 10.1 76.2 ± 10.1 78.9 ± 10.6

Prehypertension (%) 20.3 25.1 31.5 43.0 43.7 49.9 54.0 59.6

TyG-WC

SBP (mmHg) 109.8 ± 12.5 111.9 ± 13.7 115.0 ± 15.3 121.7 ± 17.6 119.6 ± 14.4 121.7 ± 14.9 123.5 ± 15.2 126.5 ± 16.0

DBP (mm Hg) 67.3 ± 9.0 68.4 ± 9.5 69.8 ± 10.1 72.8 ± 10.7 72.6 ± 9.5 74.5 ± 10.0 76.2 ± 10.1 78.7 ± 10.4

Prehypertension (%) 20.7 24.6 30.4 43.3 44.4 49.5 53.6 58.8

TyG-WHtR

SBP (mmHg) 109.8 ± 12.2 111.7 ± 13.5 114.8 ± 15.1 122.1 ± 18.0 119.4 ± 14.0 121.6 ± 14.6 123.3 ± 15.2 127.1 ± 16.5

DBP (mm Hg) 67.4 ± 8.9 68.3 ± 9.4 69.7 ± 10.0 72.8 ± 10.8 72.5 ± 9.4 74.4 ± 9.8 76.2 ± 10.1 78.9 ± 10.6

Prehypertension (%) 20.7 24.8 30.0 43.7 45.0 49.5 53.0 59.0

Note: Compared to the previous quartile, the mean value of BP and proportion of prehypertension were increased significantly, and all P < .001.
Abbreviations: BMI, body mass index; DBP, diastolic blood pressure; Q, quartile; SBP, systolic blood pressure; TyG, triglyceride and glucose index;
WC, waist circumference; WHtR, waist-to-height ratio.
 |

17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1030 ZENG et al.

F I G U R E 2 Logistic regression analysis for the associations of TyG, TyG-BMI, TyG-WC, and TyG-WHtR with prehypertension. The first
quartile of TyG and its related parameters was used as a reference; BMI, body mass index; Q, quartile; TyG, triglyceride and glucose index;
WC, waist circumference; WHtR, waist-to-height ratio

and arterial stiffness mainly in lean postmenopausal women,29 which the performance of TyG is not clear but it may have something to do
was similar to our findings that TyG was associated with prehyper- with the gender-specific differences in glycolipid metabolism, IR, and
tension only in lean women. The reason for the gender disparity of elevated BP.30,31
 |

17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ZENG et al. 1031

TA B L E 4 The AUC with its 95% CI for

Women Men
distinguishing prehypertension by obesity
indicators and combination with TyG P
Variable AUC 95% CI P values AUC 95% CI values

BMI 0.592 0.587-0.598 <.001 0.562 0.556-0.567 <.001

WC 0.595 0.589-0.600 <.001 0.556 0.551-0.562 <.001
WHtR 0.599 0.594-0.605 <.001 0.553 0.547-0.558 <.001
TyG 0.605 0.600-0.611 <.001 0.550 0.544-0.555 <.001
TyG-BMI 0.619 0.614-0.625 <.001 0.570 0.564-0.575 <.001
TyG-WC 0.618 0.612-0.623 <.001 0.565 0.559-0.570 <.001
TyG-WHtR 0.619 0.613-0.624 <.001 0.562 0.556-0.567 <.001

Abbreviations: AUC, area under the receiver operating characteristic curve; BMI, body mass index;
CI, confidence interval; TyG, triglyceride and glucose index; WC, waist circumference; WHtR,
waist-to-height ratio.

Attributing the well-validated role of obesity in IR, the integra-
tion of TyG and adiposity parameters theoretically has an advantage
to reflect IR. Lim et al and Er et al concluded that TyG-BMI was supe-
rior to TyG, TyG-WC, and TyG-WHtR for IR prediction.32,33 Another
study also demonstrated that TyG-BMI had higher OR and AUC val-
34
ues for prediabetes in Colombian men. But what about such supe-
riority among normal-weight individuals? In the present study, both
TyG-BMI and TyG-WC performed better than TyG along in both
genders. An implication of this is the possibility that combined use of
obesity indicators may increase the effectiveness of IR assessments
even in lean populations.
It is somewhat surprising that TyG-BMI performed best but
TyG-WHtR performed worst among these indicators after we had
excluded those individuals with elevated BMI. Generally, WHtR, a
marker of central adiposity, may be superior to BMI in detecting risk
factors of CVD, particularly in Asians.35 Nevertheless, some other
studies have not shown the superiority of WHtR over BMI for iden-
36,37
tifying cardiometabolic risk factors. These inconsistent results
are not only related to the differences in age, ethnicity, and gender,
but may also be related to the limited ability of WHtR to differentiate
abdominal subcutaneous and visceral fat. Therefore, we still cannot
conclude which obesity indicator is the best out of a specific con-
text, and further additional studies on TyG combined anthropomet-
ric indicators are required. (reviewer #1, comment #5).
The main strength of the present study is a relatively large sample
size. But we must also mention the limitations of this study. First, the
cross-sectional design cannot show a causal relationship between
prehypertension and TyG and its related parameters in lean individ-
uals. Second, this might be the first large-scale study exploring the
association of TyG and its related parameters with prehypertension
in lean subjects to the best of our knowledge. So rare related stud-
ies may cause a limited possible comparisons. Third, subjects of this
study might limit the generalizability of the results to other ethnic
groups.
In conclusion, TyG-BMI, incorporating TyG and obesity indica-
tors, has the potential to become a cost-effective and complemen-
tary monitor in the hierarchical management of lean prehypertensive
individuals. However, further prospective and randomized studies
will be required to confirm our findings.
C O N FL I C T O F I N T E R E S T
No conflicts of interest to disclose.
AU T H O R C O N T R I B U T I O N
All authors were involved in developing the study concept and de-
sign, data acquisition, data management, and interpretation of re-
sults. XZL established the database. ZYZ and SXL undertook the
statistical analysis of the data and wrote the manuscript. HX and XX
helped with statistical analysis. XZL and XXZ involved in designing,
editing, and review. All authors have approved the final version of
this submission.
ORCID
Xing Zhen Liu https://orcid.org/0000-0003-1382-6453
REFERENCES
1. Timmis A, Townsend N, Gale CP, et al. European Society of
Cardiology: Cardiovascular Disease Statistics 2019. Eur Heart J.
2020;41(1):12-85.
2. Lewington S, Clarke R, Qizilbash N, Peto R, Collins R. Prospective
Studies Collaboration. Age-specific relevance of usual blood
pressure to vascular mortality: a meta-analysis of individual
data for one million adults in 61 prospective studies. Lancet.
2002;360(9349):1903-1913.
3. Qi Y, Han X, Zhao D, et al. Long-term cardiovascular risk associated
with stage 1 hypertension defined by the 2017 ACC/AHA hyper-
tension guideline. J Am Coll Cardiol. 2018;72(11):1201-1210.
4. Liu XZ, Chen DS, Di FP, et al. Association between cardiovascular
risk factors and stage 1 hypertension defined by the 2017 ACC/
AHA guidelines. Clin Exp Hypertens. 2020;8:1-7.
5. Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of
the Joint National Committee on Prevention, Detection, Evaluation,
and Treatment of High Blood Pressure: the JNC 7 report. JAMA.
2003;289(19):2560-2572.
6. Whelton PK, Carey RM, Aronow WS, et al. 2017 ACC/AHA/AAPA/
ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA Guideline for
the Prevention, Detection, Evaluation, and Management of High
Blood Pressure in Adults: A Report of the American College of
 |
1032
Cardiology/American Heart Association Task Force on Clinical
Practice Guidelines. J Am Coll Cardiol. 2018;71(19):e127-e248.
7. Liu XZ, Qian JD, Li HH, et al. Body roundness index is significantly
associated with prehypertension and hypertension in nonobese
Chinese subjects. Biomed Environ Sci. 2019;32(11):854-859.
8. Neeland IJ, Poirier P, Després JP. Cardiovascular and metabolic
heterogeneity of obesity: Clinical challenges and implications for
management. Circulation. 2018;137(13):1391-1406.
9. Song R, Peng W, Zhang Y, et al. Central role of E3 ubiquitin li-
gase MG53 in insulin resistance and metabolic disorders. Nature.
2013;494(7437):375-379.
10. Simental-Mendía LE, Rodríguez-Morán M, Guerrero-Romero F. The
product of fasting glucose and triglycerides as surrogate for identi-
fying insulin resistance in apparently healthy subjects. Metab Syndr
Relat Disord. 2008;6(4):299-304.
11. Zheng S, Shi S, Ren X, et al. Triglyceride glucose-waist circumfer-
ence, a novel and effective predictor of diabetes in first-degree rel-
atives of type 2 diabetes patients: cross-sectional and prospective
cohort study. J Transl Med. 2016;14:260.
12. Landsberg L, Aronne LJ, Beilin LJ, et al. Obesity-related hyper-
tension: pathogenesis, cardiovascular risk, and treatment: a po-
sition paper of The Obesity Society and the American Society of
Hypertension. J Clin Hypertens (Greenwich). 2013;15(1):14-33.
13. Liu XZ, Fan J, Pan SJ. METS-IR, a novel simple insulin resistance
indexes, is associated with hypertension in normal-weight Chinese
adults. J Clin Hypertens (Greenwich). 2019;21(8):1075-1081.
14. Deshpande-Joshi SS, Rao S. Differential risk of hypertension among
lean and nonlean rural subjects in relation to decadal changes in
anthropometry. J Am Coll Nutr. 2018;37(5):380-386.
15. Egan BM, Stevens-Fabry S. Prehypertension–prevalence,
health risks, and management strategies. Nat Rev Cardiol.
2015;12(5):289-300.
16. Gu D, Chen J, Wu X, et al. Prehypertension and risk of cardiovascu-
lar disease in Chinese adults. J Hypertens. 2009;27(4):721-729.
17. Fukuhara M, Arima H, Ninomiya T, et al. Impact of lower range of
prehypertension on cardiovascular events in a general population:
the Hisayama Study. J Hypertens. 2012;30(5):893-900.
18. Fan J, Li HH, Huang S, Liu XZ. The prevalence of obesity and met-
abolic abnormalities in eastern China: A cross- sectional study. Int J
Diabetes Dev Ctries. 2019;39:685-691.
19. Jurik R, Stastny P. Role of nutrition and exercise programs in reduc-
ing blood pressure: a systematic review. J Clin Med. 2019;8(9):1393.
20. Arabshahi S, Busingye D, Subasinghe AK, Evans RG, Riddell MA,
Thrift AG. Adiposity has a greater impact on hypertension in lean
than not-lean populations: a systematic review and meta-analysis.
Eur J Epidemiol. 2014;29(5):311-324.
21. Zhou W, Shi Y, Li YQ, et al. Body mass index, abdominal fatness, and
hypertension incidence: a dose-response meta-analysis of prospec-
tive studies. J Hum Hypertens. 2018;32(5):321-333.
22. Jayedi A, Rashidy-Pour A, Khorshidi M, Shab-Bidar S. Body mass
index, abdominal adiposity, weight gain and risk of developing hy-
pertension: a systematic review and dose-response meta-analysis
of more than 2.3 million participants. Obes Rev. 2018;19(5):654-667.
23. Tam CS, Xie W, Johnson WD, Cefalu WT, Redman LM, Ravussin
E. Defining insulin resistance from hyperinsulinemic-euglycemic
clamps. Diabetes Care. 2012;35(7):1605-1610.
24. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF,
Turner RC. Homeostasis model assessment: insulin resistance and
beta-cell function from fasting plasma glucose and insulin concen-
trations in man. Diabetologia. 1985;28(7):412-419.
25. Manley SE, Stratton IM, Clark PM, Luzio SD. Comparison of 11
human insulin assays: implications for clinical investigation and re-
search. Clin Chem. 2007;53(5):922-932.
17517176, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jch.13878 by Cochrane Macao, Wiley Online Library on [12/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ZENG et al.
26. Mohd Nor NS, Lee S, Bacha F, Tfayli H, Arslanian S. Triglyceride
glucose index as a surrogate measure of insulin sensitivity in obese
adolescents with normoglycemia, prediabetes, and type 2 diabetes
mellitus: comparison with the hyperinsulinemic-euglycemic clamp.
Pediatr Diabetes. 2016;17(6):458-465.
27. Guerrero-Romero F, Simental-Mendía LE, González-Ortiz M, et al.
The product of triglycerides and glucose, a simple measure of in-
sulin sensitivity. Comparison with the euglycemic-hyperinsulinemic
clamp. J Clin Endocrinol Metab. 2010;95(7):3347-3351.
28. Liu XZ, Xu X, Zhu JQ, Zhao DB. Association between three non-in-
sulin-based indexes of insulin resistance and hyperuricemia. Clin
Rheumatol. 2019;38(11):3227-3233.
29. Lambrinoudaki I, Kazani MV, Armeni E, et al. The TyG Index as
a marker of subclinical atherosclerosis and arterial stiffness in
lean and overweight postmenopausal women. Heart Lung Circ.
2018;27(6):716-724.
30. Tramunt B, Smati S, Grandgeorge N, et al. Sex differences in
metabolic regulation and diabetes susceptibility. Diabetologia.
2020;63:453-461.
31. Di Giosia P, Giorgini P, Stamerra CA, Petrarca M, Ferri C, Sahebkar
A. Gender differences in epidemiology, pathophysiology, and treat-
ment of hypertension. Curr Atheroscler Rep. 2018;20(3):13.
32. Lim J, Kim J, Koo SH, Kwon GC. Comparison of triglyceride glucose
index, and related parameters to predict insulin resistance in Korean
adults: An analysis of the 2007–2010 Korean National Health and
Nutrition Examination Survey. PLoS ONE. 2019;14(3):e0212963.
33. 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(3):e0149731.
34. Ramírez-Vélez R, Pérez-Sousa MÁ, González-Ruíz K, et al. Obesity-
and Lipid-Related Parameters in the Identification of Older Adults
with a High Risk of Prediabetes According to the American Diabetes
Association: An Analysis of the 2015 Health, Well-Being, and Aging
Study. Nutrients. 2019;11(11):2654.
35. Ashwell M, Gunn P, Gibson S. Waist-to-height ratio is a better
screening tool than waist circumference and BMI for adult car-
diometabolic risk factors: systematic review and meta-analysis.
Obes Rev. 2012;13(3):275-286.
36. Xiang M, Hu H, Imai T, et al. Association between anthropometric
indices of obesity and risk of cardiovascular disease in Japanese
men. J Occup Health. 2020;62:e12098.
37. Ding J, Chen X, Bao K, et al. Assessing different anthropometric
indices and their optimal cutoffs for prediction of type 2 diabetes
and impaired fasting glucose in Asians: The Jinchang Cohort Study.
J Diabetes. 2020;12:372-384.
S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found online in the
Supporting Information section.
How to cite this article: Zeng ZY, Liu SX, Xu H, Xu X, Liu XZ,
Zhao XX. Association of triglyceride glucose index and its
combination of obesity indices with prehypertension in lean
individuals: A cross-sectional study of Chinese adults. J Clin
Hypertens. 2020;22:1025–1032. https://doi.org/10.1111/
jch.13878