This study evaluates the waist-to-height ratio (WHtR) as a predictive measure of 12-month all-cause mortality in patients with first-ever acute ischemic stroke (AIS) compared to body mass index (BMI). Findings indicate that WHtR is a superior indicator of adiposity and is associated with increased mortality rates when values are either too low or too high. The results imply that WHtR could serve as a modifiable risk factor in assessing the prognosis for AIS patients in the Mexican mestizo population.

1. Original Paper
Received: February 15, 2013
Accepted: March 18, 2013
Published online: July 13, 2013
Eur Neurol 2013;70:117–123
DOI: 10.1159/000350762
Central Adiposity and Mortality after
First-Ever Acute Ischemic Stroke
Erwin Chiquete a José L. Ruiz-Sandoval c Luis Murillo-Bonilla e
Carolina León-Jiménez g Bertha Ruiz-Madrigal d, f Erika Martínez-López d, f
Sonia Román d, f Arturo Panduro d, f Alma Ramos b Carlos Cantú-Brito a
a
Department of Neurology and Psychiatry, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, and
Scientific Area, Sanofi-Aventis, Mexico City, Departments of c Neurology and d Molecular Biology, Hospital Civil de
Guadalajara ‘Fray Antonio Alcalde’, e Departments of Neurology, Facultad de Medicina, Universidad Autónoma de
Guadalajara, and f Department of Molecular Biology, Centro Universitario de Ciencias de la Salud, Universidad de
Guadalajara, Guadalajara, and g Department of Neurology, Hospital Valentín Gomez Farías, Zapopan, Mexico
b
Abstract
Background: The waist-to-height ratio (WHtR) may be a better adiposity measure than the body mass index (BMI). We
evaluated the prognostic performance of WHtR in patients
with acute ischemic stroke (AIS). Methods: First, we compared WHtR and BMI as adiposity measures in 712 healthy
adults by tetrapolar bioimpedance analysis. Thereafter,
baseline WHtR was analyzed as predictor of 12-month allcause mortality in 821 Mexican mestizo adults with first-ever
AIS by a Cox proportional hazards model adjusted for baseline predictors. Results: In healthy individuals, WHtR correlated higher than BMI with total fat mass and showed a higher accuracy in identifying a high percentage of body fat (p <
0.01). In AIS patients a U-shaped relationship was observed
between baseline WHtR and mortality (fatality rate 29.1%).
On multivariate analysis, baseline WHtR ≤0.300 or >0.800 independently predicted 12-month all-cause mortality (hazard ratio 1.91, 95% confidence interval 1.04–3.51). BMI was
© 2013 S. Karger AG, Basel
0014–3022/13/0702–0117$38.00/0
E-Mail karger@karger.com
www.karger.com/ene
not associated with mortality, tested either as continuous,
binomial or stratified variable. Conclusion: WHtR is a modifiable risk factor that accurately demonstrates body fat excess.
Extreme WHtR values were associated with increased
12-month all-cause mortality in Mexican mestizo patients
with AIS. No survival advantage was found with high WHtR
as the pragmatic indicator of obesity in this population.
Copyright © 2013 S. Karger AG, Basel
Introduction
Obesity is a well-recognized risk factor for acute ischemic stroke (AIS) [1, 2], however when BMI is tested as
predictor of mortality in people with atherothrombotic
complications such as myocardial infarction, stroke or
heart failure, a high body mass index (BMI) has been associated with a survival advantage (the so-called obesity
paradox) [3–6].
BMI is an index of both lean and fat tissues (i.e. total
body mass) as a function of height squared and therefore
BMI is not the ideal indicator of obesity [7, 8]. Other anthropometric measures, such as the waist-to-height ratio
Dr. Carlos Cantú-Brito
Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán
Vasco de Quiroga 15
Tlalpan, Mexico City, CP 14439 (Mexico)
E-Mail carloscantu_brito @ hotmail.com
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Key Words
Adiposity · Body composition · Body fat · Body mass index ·
Obesity paradox · Overweight · Stroke

2. Methods
We compared WHtR, BMI and other anthropometric measures as references of body adiposity in healthy adults in order to
find the best adiposity index of general adiposity that can be applied in AIS patients to evaluate whether the excessive body fat is
a predictor of 12-month all-cause mortality.
To find the best anthropometric measure of body adiposity, a
total of 712 Mexican mestizo adults without a history of stroke
were invited to receive body composition evaluation at the Department of Molecular Biology in Medicine, Hospital Civil de Guadalajara ‘Fray Antonio Alcalde’, Guadalajara, Mexico. The institutional committee of ethics of the Hospital Civil de Guadalajara
approved this part of the study. Informed consent was required for
all subjects. These individuals underwent evaluation by means of
bioimpedance analysis (BIA) with a computerized multifrequency
tetrapolar 8-point tactile electrode BIA system (Inbody 720; analyzing software: Inbody 3.0; Biospace Co., Ltd, Seoul, Korea). Participating subjects were evaluated in the morning, with cotton underwear without metal or synthetic textiles, in overnight fasting
and having evacuated bladder and rectum. The individuals were
asked to remove their clothes, excepting underwear, and they were
provided with a disposable cotton-made coat for use during BIA.
Hands and soles were cleaned up and impregnated with an electrolyte solution. BMI was calculated as weight (kg) divided by
height (m). WHtR was calculated as waist circumference (WC)
(cm) divided by height (cm), by using the waist measurement of
the narrowest point between the lower costal border and the top of
the iliac crest. Waist-to-hip ratio (WHR) was calculated as WC
(cm) divided by the hip circumference (cm). Body fat and lean
mass content were estimated by using the standard built-in prediction algorithms for adults (Biospace Co., Ltd.).
Among 1,376 participants with AIS or transient ischemic attack (TIA) registered in the PREMIER study [8, 10–12], a total of
821 first-ever AIS patients with complete anthropometric evaluations and 12-month follow-up outcome information were selected
for this part of the study. TIA cases were not included in this analysis. A central institutional review board and the local committee
of ethics of each participating center approved the study. In brief,
consecutive patients with AIS or TIA aged ≥18 years were included. All patients received medical care within 7 days of AIS onset.
Data collection was prospectively performed during 1 year (in six
planned research visits) by using a standardized structured questionnaire outlined in a procedure manual. All participating physicians were instructed on stroke guidelines, classification and management. Stroke subtypes were registered according to Trial of
ORG 10172 in Acute Stroke (TOAST) and Oxfordshire Community Stroke Project (OCSP) classifications. AIS severity was assessed by the National Institutes of Health Stroke Scale (NIHSS) at
118
Eur Neurol 2013;70:117–123
DOI: 10.1159/000350762
baseline, and the modified Rankin scale (mRS) was used to evaluate the functional outcome at hospital discharge, 30 and 90 days,
6, and 12 months after AIS (the six research visits). Weight, height,
and WC were measured at baseline by direct assessment with
scales, stadiometer or flexible metric rulers, with standard procedures for either supine or stand-up positions, as corresponded.
Hip circumference was not measured in this cohort. BMI and
WHtR were calculated as described above. The investigator ascertained every fatality case either directly during hospitalization, or
at each follow-up visit by telephone interview with caregivers. The
exact day of death was recorded. The information of the standardized structured questionnaires was saved on independent electronic files in data capture software developed and revised periodically
by a contract research organization (CRO; Innoval Co.). Members
of the CRO analyzed information on every patient for completeness and plausibility. Missing or implausible variables were referred to the investigator for clarification. Data quality was ascertained by periodic statistical reports and clinical site visits by CRO
monitors.
Parametric continuous variables are expressed as geometric
means and standard deviations (SD), or minimum and maximum. Non-parametric continuous variables are expressed as medians and interquartile range (IQR). Categorical variables are expressed as percentages. To compare quantitative variables distributed between two groups, Student’s t test and Mann-Whitney
U test were performed in distributions of parametric and nonparametric variables, respectively. χ2 statistics were used to compare nominal variables in bivariate analyses. Pearson’s ρ correlation was used to test the continuous association between two
quantitative variables. An r-to-z transformation was performed
to calculate a ‘z’ score that can be applied to assess the significance
of the difference between two correlation coefficients. Different
WHtR, BMI cutoffs, NIHSS cutoffs, and demographic as well as
clinical variables were tested as predictors of 12-month all-cause
mortality in univariate analyses. Variables significantly associated with mortality were selected to integrate a multivariate prediction model. Kaplan-Meyer survival estimates and Cox proportional hazards models at 12-month follow-up were constructed
to find independent baseline risk factors for all-cause mortality
after AIS, testing the WHtR and BMI cutoffs selected in univariate analyses. Multivariate hazard ratios (HR) and their respective
95% confidence intervals (CI) are provided. In healthy subjects,
BMI, WC and WHtR were evaluated by a receiver-operating
characteristic (ROC) curve for discrimination of a percentage of
body fat (%BF) >20 and >30, regarding as superior the index with
the largest area under the curve (AUC) without overlapping 95%
CIs. All p values are two-sided and considered significant when
p < 0.05. SPSS version 17.0 software was used for all statistical
calculations.
Results
WHtR Is Better than BMI as an Index of Adiposity
A total of 712 healthy adults (mean age 38.2, median
38, IQR 28–45 years; 60.5% women) underwent BIA for
body composition assessment. Significant differences
were observed between men and women with respect to
Chiquete et al.
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(WHtR), may denote more precisely the excess of body
adiposity [9]. Growing evidence suggests that WHtR is
stronger than BMI as a risk factor for stroke [2]. In this
study we tested the hypotheses that WHtR is better than
BMI as an index of adiposity in healthy adults and stronger than BMI as predictor of death in Mexican patients
with a first-ever AIS.

3. Color version available online
80
60
40
AUC (95% CI)
WHtR: 0.908 (0.883–0.932)
BMI: 0.769 (0.729–0.810)
WC: 0.808 (0.771–0.845)
WHR: 0.775 (0.734–0.816)
20
0
0
a
20
40
60
80
100
False positives (%)
True positives (%)
100
80
True positives (%)
100
60
40
AUC (95% CI)
WHtR: 0.961 (0.949–0.973)
BMI: 0.889 (0.866–0.912)
WC: 0.907 (0.886–0.928)
WHR: 0.842 (0.812–0.872)
20
0
0
20
b
40
60
80
100
False positives (%)
Mexican mestizo adults who underwent tetrapolar BIA. b ROC
curve on the discriminatory function of anthropometric indices
for %BF >30.
Table 1. Univariate Pearson’s correlation of several indices of adi-
mean %BF (27.7 vs. 31.8%, respectively; p < 0.001), BMI
(28.5 vs. 25.9, respectively; p < 0.001), WC (93.6 vs. 89.3
cm, respectively; p = 0.001) and WHR (0.880 vs. 0.890,
respectively; p = 0.03), but not with respect to age (38.6
vs. 38.0 years, respectively; p = 0.52) or, more importantly, the WHtR (0.550 vs. 0.560, respectively; p = 0.53). In
healthy adults, WHtR correlated significantly higher
than BMI with total body fat within each BMI interval
(table 1). Moreover, WHtR showed higher accuracy than
BMI, WC or WHR in identifying both a %BF >20 or >30
(fig. 1a, b).
WHtR Is a Predictor of 12-Month All-Cause Mortality
after a First-Ever AIS
A total of 821 Mexican mestizo patients with AIS (52.6%
women, mean age 67.9, median 70, IQR 57–79 years) were
analyzed for the association of baseline adiposity measures
with 12-month all-cause mortality (table 2). At the
12-month follow-up, a total of 90 (11.0%) patients achieved
a mRS = 0; 191 (23.3%) had a mRS = 1; 109 (13.3%) had a
mRS = 2; 89 (10.8%) had a mRS = 3; 74 (9.0) had a mRS =
4; 29 (3.5%) had a mRS = 5, and 239 (29.1%) patients died.
A U-shaped relationship was observed between WHtR intervals and 12-month all-cause mortality risk (fig. 2a), so
that both low or high baseline WHtR measurements were
associated with an increased 12-month mortality rate. Notably, mean BMI increased as a function of WHtR, but BMI
ranges significantly overlapped across WHtR intervals
(fig. 2a). An inverse relationship was found between the
frequency of hypercholesterolemia and 12-month allcause mortality (table 2), possibly explained by the higher
use of statins among patients with dyslipidemia than
among non-dyslipidemic individuals (9.1 vs. 5.2%, respectively; p = 0.04). Kaplan-Meier estimates showed a significantly lower survival in patients with baseline WHtR
≤0.300 or >0.800 (fig. 2b). Differences in mortality rates
were significant since the first 6 months after AIS (p =
0.03). In a multivariate analysis by the Cox proportional
hazards method adjusted for relevant baseline confounders (table 3), WHtR ≤0.300 or >0.800, age >65 years, to-
Central Adiposity and Mortality in Acute
Stroke
Eur Neurol 2013;70:117–123
DOI: 10.1159/000350762
posity with %BF, according to BMI strata, in 712 healthy adults
who received tetrapolar BIAa
Characteristic BMI <20 BMI 20–25 BMI 25.1–30 BMI >30
(n = 48) (n = 285)
(n = 197)
(n = 182)
WHtR
BMI
WC
WHR
0.773b
0.401b
0.614b
0.597b
0.702b
0.237b
0.396b
0.355b
0.864b
0.460b
0.557b
0.530b
–0.715b
–0.666b
–0.423b
–0.026
a p < 0.05 for comparison of Pearson’s correlation between BMI
and total body fat with that of WHtR and total body fat.
b p < 0.001 for significance of univariate Pearson’s correlation.
119
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Fig. 1. Accuracy of anthropometric measures in identifying excessive adiposity in healthy adults. a ROC curve on the discriminatory function of anthropometric indices for %BF >20 in 712 healthy

4. Table 2. Main characteristics of patients with a first-ever acute cerebral infarction (n = 821) and their association with 12-month allcause mortality
Variable
12-Month all-cause mortality
absent (n = 582)
Median age, years
Male
NIHSS at hospital admission, median
Major vascular risk factors
Hypertension
Diabetes mellitus
Hypercholesterolemia
Atrial fibrillation
Coronary artery disease
Heart failure
Past or current smoking
Ischemic stroke syndromes
Total anterior circulation cerebral infarction
Partial anterior circulation cerebral infarction
Lacunar cerebral infarction
Posterior circulation cerebral infarction
Ischemic stroke mechanisms
Large-artery atherothrombosis
Lacunar
Cardioembolism
Mixed mechanism
Other determined mechanisms
Undetermined mechanism
Baseline anthropometric measures
Weight, kg
Height, m
WC, cm
WHtR
Body mass index
>25
>27
>30
>35
68.0 [56.0–77.0]
282 (48.5)
8.0 [5.0–13.0]
p value
present (n = 239)
77.00 [65.0–85.0]
107 (44.8)
19.0 [14.0–26.5]
373 (64.1)
199 (34.2)
136 (23.4)
44 (7.6)
70 (12.0)
40 (6.9)
212 (36.4)
157 (65.7)
84 (35.1)
29 (12.1)
46 (19.2)
36 (15.1)
38 (15.9)
93 (38.9)
54 (9.3)
238 (40.9)
190 (32.6)
100 (17.2)
119 (49.8)
72 (30.1)
13 (5.4)
35 (14.6)
56 (9.6)
140 (24.1)
91 (15.6)
33 (5.7)
35 (6.0)
227 (39.0)
9 (3.8)
12 (5.0)
65 (27.2)
12 (5.0)
9 (3.8)
132 (55.2)
71.8±4.6
1.62±0.09
93.3±15.4
0.577±0.096
27.35±4.66
406 (69.8)
290 (49.8)
138 (23.7)
30 (5.2)
70.4±15.3
1.61±0.09
93.7±17.4
0.584±0.105
27.19±5.20
153 (64.0)
120 (50.2)
62 (25.9)
15 (6.3)
<0.001
<0.34
<0.001
<0.66
<0.79
<0.001
<0.001
<0.24
<0.001
<0.50
<0.001
<0.001
<0.19
<0.10
<0.75
<0.41
<0.67
<0.11
<0.92
<0.50
<0.52
Values are mean ± SD, n (%) or IQR in brackets.
Discussion
When compared with BMI these results demonstrate
that WHtR is a better measure of adiposity and a stronger
predictor of 12-month all-cause mortality in Mexican
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DOI: 10.1159/000350762
mestizo patients with AIS. We found a U-shaped relationship between WHtR and mortality, and therefore did
not observe any protective effect of a high BMI or high
WHtR in this first-ever AIS cohort.
WHtR has been traditionally considered an anthropometric measure of central adiposity adjusted for a given
height [7, 9]. Here we show that WHtR can accurately
indicate general adiposity as well. Central adiposity has
been found to be associated with an adverse metabolic
profile that traduce into a high cardiovascular risk [9]. If
WC parallels with increments of visceral fat tissue when
weight gain occurs at the expense of positive energy balChiquete et al.
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tal anterior circulation cerebral infarction syndrome, and
NIHSS were significant predictors of 12-month all-cause
mortality (table 3). BMI was not significantly associated
with 12-month mortality, tested either as a continuous, binomial or stratified variable (table 3).

5. 2
20
0
0
Deaths, n
Number at risk
a
BMI
Mean
SD
Range
100
80
WHtR 0.301–0.800
60
40
WHtR
20
Fig. 2. All-cause mortality after a first-ever
AIS. a One-year all-cause mortality ac-
cording to baseline WHtR: in circles, relative frequency; in triangles, age- and sexadjusted HRs. The corresponding BMI for
every WHtR interval is also shown. b Kaplan-Meier estimates according to baseline
WHtR ≤0.300 or >0.800. Rhombuses indicate censored cases.
0
Number at risk
WHtR 0.301–0.800
b WHtR
0
802
19
100
200
300
Days after first-ever AIS
614
11
593
10
400
570
8
As reflected by WHtR, in the present study both a reduced and an excessive central adiposity increase the
probability of death after a first-ever cerebral infarction.
Indeed, on the one hand it is possible that certain energy
stores are necessary to cope with metabolic demands that
follow AIS [8, 13, 14], and on the other hand, an excessive
visceral fat could be associated with an adverse risk profile. When analyzing a high BMI as a predictor of mortality in subjects who have survived an atherothrombotic
Central Adiposity and Mortality in Acute
Stroke
Eur Neurol 2013;70:117–123
DOI: 10.1159/000350762
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ance, then WHtR may denote more accurately the most
important body mass in terms of chronic risks. Both
obese and muscled persons can have the same BMI if
weight (with different proportions of lean and fat masses)
and height are the same, but with radically different risks.
On the other hand, WC does not increase significantly in
muscled individuals; hence, the adjustment of WC for
height provides the opportunity of correcting central adiposity for variations of height.

6. Table 3. Multivariate analysis on baseline factors associated with
12-month all-cause mortality in patients with a first-ever acute cerebral infarction (n = 821): a Cox proportional hazards modela
Predictor
HR (95% CI)
p value
TACI
NIHSSb
WHtR ≤0.300 or >0.800
Agec
2.435 (1.759−3.371)
2.182 (1.751−2.720)
1.911 (1.040−3.514)
1.018 (1.008−1.027)
<0.001
<0.001
<0.037
<0.001
a
Adjusted for atrial fibrillation, hypercholesterolemia, statin
use, heart failure, stroke mechanisms, stroke syndromes, BMI
(tested as a continuous, stratified or binomial variable with different cutoffs), WC and total body weight.
b
NIHSS <9, 9–18 and >18 points.
c
Age per 1-year increment.
complication (i.e. stroke, myocardial infarction, heart
failure, and other complications), it can be erroneously
concluded that obesity provides a survival advantage, a
concept that may be misinterpreted by the general population, with potential negative consequences for public
health.
Our findings are in conflict with the obesity paradox
concept. In a previous analysis of the PREMIER cohort,
we originally found that a high BMI was apparently associated with a good functional outcome in stroke survivors exclusively [8], confirming the obesity paradox in
the context of functional recovery. However, when WHtR
was analyzed as a measure of adiposity excess (i.e. obesity), no functional advantage was found with high WHtR
or high BMI in adjusted multivariate analyses [8]. It is
possible that the elimination of patients with a previous
stroke can reduce the bias of survival selection for the
obese individuals, then reducing the apparent advantage
with high BMI values. In other words, it remains unquestionable that a high BMI is strongly associated with increased mortality and cardiovascular risks [15–17], but
when studying persons who already have a cardiovascular
event, and the onset of such an event is the new ‘zero
point’ for mortality analysis, the inclusion of obese patients who had survived several cardiovascular events
may bias towards the selection of strong body constitutions that may be more ‘resistant’ to the metabolic challenges after atherothrombotic events in the long run. So
far, no indisputable explanation to the obesity paradox
concept has been put forward [18].
The main limitation of our study is the lack of direct
body composition analysis in the cohort with AIS, which
would allow for estimation of the exact predictive value
of adiposity in diseased persons. Another limitation is the
relatively small sample size that might hamper robust
analyses. At the population level different WHtR cutoffs
may apply in terms of long-term cardiometabolic risks, if
we consider that the present study was only about patients with arterial disease at baseline. Given the body
composition characteristics of the Mexican mestizo population, our findings should be tested in different bioethnic groups and other forms of cerebrovascular and cardiometabolic diseases.
In conclusion, extreme WHtR values are modestly, but
significantly associated with an increased all-cause mortality risk in Mexican mestizos, in the late part of the evolution after a first-ever AIS. These findings should be retested in different scenarios.
Disclosure Statement
This study received unrestricted funds from Sanofi-Aventis for
the registering of patients with stroke. The company did not participate, either directly or indirectly in study design, selection of
patients, data analysis, manuscript draft or the decision to summit
for publication.
Mrs. A. Ramos is employed by Sanofi-Aventis, Mexico, in the
Clinical Research Area, and Dr. C. Cantú-Brito served in the Scientific Advisory Board of the PREMIER Registry. None of the other authors have any conflicts of interest to disclose.
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