Review Article

Is Metabolic Syndrome Associated with the Risk of Recurrent

Stroke: A Meta-Analysis of Cohort Studies

,1
Xuelong Li, PhD,*Xianliang Li, PhD,*,1 Fang Fang, PhD,† Xian Fu, PhD,*
Hualiang Lin, PhD,‡ and Qingchun Gao, PhD*

Background: The association between metabolic syndrome (MetS) and recurrence

of stroke remains unknown. We summarized the evidence by a meta-analysis of
prospective cohort studies. Methods: We searched the PubMed, EMBASE, and Google
Scholar databases from their inception until July 2016 for cohort studies investi-
gating this research question; relevant information was extracted by 2 independent
investigators, and then aggregated using the random-effects meta-analysis approach.
Results: We identified 5 studies, including 7752 stroke patients who had a history
of stroke or transient ischemic attack. Compared with persons without MetS, persons
with MetS have a significantly higher risk of recurrent stroke, and the pooled rel-
ative risk (RR) was 1.52 (95% confidence interval (CI): 1.17-1.97). The strength of
this association is greater than individual MetS components such as elevated blood
pressure (RR = 1.05, 95% CI: .72-1.52), elevated triglycerides (RR = 1.04, 95% CI:
.84-1.29), low high-density lipoprotein cholesterol (RR = 1.16, 95% CI: .91-1.48), or
obesity (RR = 1.12, 95% CI: .89-1.41). The risk of recurrent stroke was highest in
the group with elevated glycemia (RR = 1.70, 95% CI: 1.12-2.56). Conclusions: This
meta-analysis suggests that MetS might be an important predictor of recurrent
stroke. Among the 5 components of MetS, elevated glycemia was a stronger pre-
dictor for recurrent stroke. Key Words: Metabolic syndrome—recurrent
stroke—cardiovascular diseases—meta-analysis.
© 2017 National Stroke Association. Published by Elsevier Inc. All rights reserved.

Introduction Previous studies showed that persons who survived

a stroke or transient ischemic attack (TIA) are at higher
Being an increasing important public health concern, risk of experiencing recurrent stroke.2,3 In the United States,
stroke ranks as the third leading cause of death and the about one fourth of the nearly 800,000 strokes each year
first cause of disability in most countries around the world.1 are recurrent cases.4 The situation is much worse in China;

From the *Institute of Neuroscience, The Second Affiliated Hospital, Guangzhou Medical University, Guangzhou, China; †College for Public
Health and Social Justice, Saint Louis University, Saint Louis, Missouri; and ‡Guangdong Provincial Institute of Public Health, Guangdong
Provincial Center for Disease Control and Prevention, Guangzhou, China.
Received November 21, 2016; revision received February 22, 2017; accepted March 12, 2017.
Grant support: This study was funded by the National Natural Science Foundation of China (Grant No.: 81371573) and Science and Tech-
nology Planning Project of Guangdong Province (Grant No.: 2014A020212328).
Address correspondence to Qingchun Gao, PhD, Institute of Neuroscience, The Second Affiliated Hospital, Guangzhou Medical University,
No. 250 Chang Gang East Road, Guangzhou, Guangdong, China. E-mail: qcgao@263.net.
1
These authors contributed equally as first authors.
1052-3057/$ - see front matter
© 2017 National Stroke Association. Published by Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.03.014

2700 Journal of Stroke and Cerebrovascular Diseases, Vol. 26, No. 12 (December), 2017: pp 2700–2705

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METABOLIC SYNDROME AS PREDICTOR OF RECURRENT STROKE 2701
1 long-termed epidemiologic study reported that the in- ative risks (RRs) with 95% confidence intervals (CIs) or
cidence of stroke has increased in China and one third reported outcomes as count data; (3) participants with
of stroke cases were recurrent strokes.5 Consequently, rec- stroke or TIA at baseline were included; (4) the study
ognition of patients at high risk of recurrence and should have evaluated the association between MetS and
secondary stroke prevention continues to be a challenge recurrent stroke risk. Studies not meeting these criteria
and great concern to clinicians. were excluded.
Metabolic syndrome (MetS) is mainly characterized by
impaired glucose tolerance, elevated blood pressure, dys- Data Extraction and Quality Assessment
lipidemia, and central obesity.6 Previous studies have consis-
Two investigators performed data extraction indepen-
tently demonstrated a significant association between MetS
dently, and any disagreements were adjudicated through
and incidence of ischemic stroke.7,8 Guidelines for preven-
discussion to reach a third reviewer. The following in-
tion of stroke in patients with ischemic stroke or TIA
formation was extracted from each study: (1) first author’s
published in 2014 proposed that MetS can predict cardio-
name; (2) year of publication; (3) country of origin; (4)
vascular diseases and subsequent mortality.9 However, it re-
age, sex, and race distribution, and MetS prevalence of
mained unknown whether MetS is a predictor of recurrent
the study population; (5) duration of follow-up; and (6)
stroke events in patients with a history of stroke or TIA.
MetS criteria. For this study, we selected all the publi-
In recent years, a few studies have been conducted to
cations with various definitions of MetS from the following
assess the association between MetS and the recurrence
panels or organization, including the Third Report of the
risk of stroke10,11; however, the findings have been in-
Expert Panel on Detection, Evaluation, and Treatment of
consistent. Liu et al12 found that MetS itself may not be
High Blood Cholesterol in Adults (Adult Treatment Panel
predictive of the short-term prognosis of patients, whereas
III), International Diabetes Federation, Health Organiza-
hyperglycemia is a significant predictor of poor func-
tion, and the American Heart Association, or other widely
tional outcomes. However, Fang et al13 showed that the
accepted definitions for MetS. Quality assessment for cohort
risk of recurrent stroke was 43% higher in MetS pa-
studies was assessed using the Newcastle Ottawa scale
tients than in non-MetS patients. On the other hand, studies
(NOS), which, if it met 5 or less, was deemed as low; 6
with small sample size of participants might be of limited
and 7, moderate; and 8 and 9, high level of quality. The
statistical power to assess the effect, and results from these
study selection process was depicted diagrammatically
studies have not been summarized with a meta-analysis.
in Figure 1.
Given the high and increasing prevalence of MetS and
the persisting controversy, clarifying this issue has im-
Statistical Analyses
portant public health and clinical significance. We, therefore,
conducted a systematic review and meta-analysis to In this meta-analysis, we used recurrent stroke as the
examine whether MetS and its individual components were study outcome. The results of each cohort study were
associated with increased recurrent stroke risk. reported as RR or hazard ratio. Homogeneity was tested
by the Q statistic (significance level at P < .10) and the

Methods
Literature Search Articles identified through database searching (n=1509)

Papers were identified by searching PubMed, EMBASE,

Google Scholar databases, and the conference proceed-
ings of the international stoke conference from their Articles after duplicates removed (n=620)
inception until June 2016 using the following MeSH terms
or key words: metabolic syndrome, syndrome X, cardio-
Articles excluded based on titles and abstracts (n=852)
vascular risk, cardiovascular disease, stroke or transient
ischemic attack, cohort studies. No language restric-
tions were imposed on publications. Besides, a manual Full text articles reviewed (n=37)
search of citations from relevant original studies and review
articles was also performed for additional studies not iden-
Articles excluded based on (n=32):
tified in the literature search. Moreover, additional data
Unrelated (n=22)
required for this study were obtained by contacting the
authors of the included studies. Comment (n=5)

Cross-sectional studies (n=5)

Study Selection
Articles met inclusion criteria (n=5)
Studies meeting the following criteria were included
in the meta-analysis: (1) cohort studies; (2) reported rel- Figure 1. Flow diagram of literature search and study selection.

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2702 X. LI ET AL.
I statistic (significance level at I >50%), the pooled risk
2 2

estimates were computed using either fixed-effects models

(I2 <50.0%) or, in the presence of heterogeneity (I2 >50.0%),
random-effects models. Sensitivity analyses tested whether
the results could have been affected by a single study.
We also performed Begg’s and Egger’s tests to evaluate
the presence of publication bias. All analyses were per-
formed using R software (Bell Laboratories).

Results
Literature Search
The flow diagram of literature search and study se-
lection is shown in Figure 1. The reason for exclusion
was that the studies were published as letters, com-
ments, reviews, meta-analyses, or conference abstracts.
Initially we retrieved 1785 articles from the PubMed, 1593
articles from the EMBASE, 1046 articles from the Google
Scholar databases, and 5 articles from the conference pro-
ceedings of the International Stoke Conference. Of 1509
references obtained after execution of the search strate-
gy, 37 were found to be relevant after removing duplicates
and screening titles and abstracts. Five cohort studies were
finally included in this meta-analysis.11-15
Study Characteristics
Table 1 summarizes the various characteristics of in-
cluded studies. The included 5 cohort studied consisted
of 7752 participants. Of them, 2 studies were conducted
in the United States, 3 were in China. The study samples
ranged from 476 to 2999, and the follow-up durations
ranged from 90 days to 4.5 years. The included studies
were published between 2006 and 2016. The number of
potential confounding factors included in the adjusted
analyses varied; age, sex, and smoking behavior was ad-
justed for as confounding factors in most studies. All studies
reported results of prevalence of MetS for both men and
women but did not report sex-specific estimate RR results.
Most studies included both men and women >60 years
old. The included studies have moderate to high quality,
with quality scores ranging from 7 to 9 points.
The Metabolic Syndrome and Risk of Recurrent Stroke
The RR of recurrent stroke risk associated with the MetS
in each study and overall is shown in Figure 2. No sta-
tistically significant heterogeneity across studies was found
(P = .730, I2 = 0%). MetS was associated with a signifi-
cant increased stroke recurrence risk in all studies (RR,
1.52; 95% CI: 1.17-1.97; P = .0015).
Individual Components of Metabolic Syndrome and
Their Risk for Recurrent Stroke
As shown in Table 2, the strength of this association
is greater than MetS individual components such as el-
Figure 2. Hazard ratios of recurrent stroke risk associated with the MetS.
Abbreviations: CI, confidence interval; HR, hazard ratio; Lci, lower con-
fidence interval; MetS, metabolic syndrome; RE model, Randomization model;
Uci, upper Confidence interval.
evated blood pressure (RR = 1.05, 95% CI: .72-1.52), elevated
triglycerides (RR = 1.04, 95% CI: .84-1.29), low high-
density lipoprotein cholesterol (RR = 1.16, 95% CI: .91-
1.48), or obesity (RR = 1.12, 95% CI: .89-1.41). The risk
of recurrent stroke was highest in the group with el-
evated glycemia (RR = 1.70, 95% CI: 1.12-2.56).
Analysis of Heterogeneity and Publication Bias
The subgroup analyses by study location (China and
the United States) were conducted. No significant asso-
ciations between MetS and their risk for recurrent stroke
were identified in the subgroup analyses (Table 3). A sen-
sitivity analysis of omitting 1 study in each turn did not
markedly change the results, indicating robust main meta-
analysis results. Egger’s test revealed that there was no
publication bias in studies (z = −.20, P = .84).
Discussion
Recurrent stroke has been recognized as a leading cause
of disability and mortality for stroke patients.16 MetS is
a series of metabolic disorders including elevated gly-
cemia, central obesity, dyslipidemia, and hypertension that
was first recognized with an international definition in
1998. In the past few years, the role of MetS on the de-
velopment of stroke recurrence has been explored
extensively. However, the findings were controversial and
the potential significance of MetS in predicting recur-
rent stroke is not well documented. Our study provides
further evidence to suggest that MetS may be associ-
ated with early recurrent stroke in stroke patients.
To our knowledge, this meta-analysis was the first to
examine the association between the MetS and recur-
rent stroke risk. The findings from this meta-analysis of
5 cohort studies indicated that MetS was associated with
a 52% increase in recurrent stroke risk overall, and the
prevalence of MetS varied from 32% to 58.3%. Besides,
of the 5 components of the MetS, elevated glycemia was
an independent predictor for recurrent stroke.

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 METABOLIC SYNDROME AS PREDICTOR OF RECURRENT STROKE
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Table 1. Characteristics of studies included in the meta-analysis

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Prevalence Prevalence
Study of metabolic of metabolic Definition
sample Recurrent syndrome syndrome Duration of of metabolic Quality
Study, year Country size Age stroke (female) (male) follow-up syndrome scores Adjustment

Ovbiagele et al 200611 USA 476 63.0 ± 11.4 — 97 (53%) 107 (37%) 1.8 years NCEP-ATP III 7 None
Mi et al 201214 China 2639 — 195 59 (44.2%) 75 (55.8%) 1 year IDF 8 Age, sex, smoking behavior,
history of atrial fibrillation
and coronary heart disease,
NIHSS, medication with
antihypertensive and
hypoglycemic drugs in
hospital.
Fang et al 201613 China 1087 65.1 ± 8.9 143 226 (42.6%) 213 (48.5%) 4.5 years CDS 9 Age, gender, education,
marriage status, subtype
stroke, times of stroke,
history of cardiac diseases,
smoking status, drinking
status, clinics, aspirin use,
fibrinogen, months of
index stroke to baseline
assessment.
Zhu et al 201515 USA 2999 62.1 ± 9.7 274 380 (34%) 567 (30%) 3.8 years AHA/NHLBI WHO 8 None
Liu et al 201512 China 530 69.3 ± 11.2 51 156 (70.3%) 153 (49.7%) 90 days AHA/NHLBI 8 Age and sex

Abbreviations: AHA/NHLBI, American Heart Association/National Heart, Lung, and Blood Institute; CDS, Chinese Diabetes Society; IDF, International Diabetes Federation; NCEP-ATP III,
National Cholesterol Education Programs-Adult Treatment Panel III; NIHSS, National Institutes of Health Stroke Scale; WHO, World Health Organization.

2703
2704
Table 2. Individual components of metabolic syndrome and their risk for recurrent stroke
Components of metabolic syndrome Number of studies/patients
Elevated blood pressure
Elevated glycemia
Elevated triglycerides
Low HDL cholesterol
Obesity
Abbreviation: HDL, high-density lipoprotein.
Several MetS definitions have been proposed by dif-
ferent organizations over the past decade, and the
definitions of National Cholesterol Education Programs
III, International Diabetes Federation, and the World
Health Organization are the most commonly used. Four
studies we included on the relation between MetS and
recurrent stroke were based on these criteria, which
make the results comparable among these studies. There
was also 1 study that used the Chinese Diabetes Society
criteria, which were released by the Chinese Medical
Association of Diabetes in 2004. Waist circumference is
not a component, and body mass index replaced waist
circumference in the criteria. A 10-year follow-up cohort
study from 30,378 middle-aged Chinese adults showed
that the risks of ischemic cardiovascular diseases or
stroke were similar in those with and without central
obesity. We believe that it is unlikely altering the results
of the study when they used the Chinese Diabetes
Society definition.
Diabetes is at epidemic proportion worldwide; the effects
of diabetes on the risk of stroke among individuals without
a prior cerebrovascular event were well established.17,18
However, the effect of diabetes on the risk of recurrent
cerebrovascular events appears to be less than those that
are reported for first events. In our study, elevated gly-
cemia is a robust predictor of recurrent stroke. This is
consistent with the results of epidemiologic studies that
have evaluated the association between diabetes and stroke
recurrence.19-21 In a previous Chinese National Stroke Reg-
istry study, patients with diabetes had a significantly higher
incidence of recurrent stroke at 3 and 6 months after stroke
onset.22 Because stroke is the leading cause of death in
patients with diabetes, strategies to reduce stroke recur-
rence through better glycemic control have to be tested
Table 3. Results of subgroup analyses
Subgroup Number of studies Hazard rate
Countries
USA 2 1.66
China 3 1.42
Abbreviation: CI, confidence interval.
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X. LI ET AL.
Hazard rate (95% CI) P
4 1.05 (.72, 1.52) .79
4 1.70 (1.12, 2.56) .01
4 1.04 (.84, 1.29) .71
4 1.16 (.91, 1.48) .22
4 1.12 (.89, 1.41) .32
in clinically relevant end points. However, there remain
many debates as to whether the MetS used as a predic-
tor of stroke recurrence offers any advantages over its
individual components. This meta-analysis of individu-
al components was done to explore the differential effect
of individual components in the presence of MetS. Al-
though elevated triglycerides, elevated glycemia, and low
high-density lipoprotein cholesterol levels have been pre-
viously associated with increased recurrent stroke risk,23
these factors are often overlooked in clinical practice. Our
results suggest that these factors could also be potential
targets for reducing the risk of stroke recurrence events,
whereas only the elevated glycemia was a stronger pre-
dictor for recurrent stroke, and other factors are not closely
related. This is not consistent with the results of most
studies. This might be explained by the following 2 reasons:
(1) too few studies were included; and (2) some of the
studies that were included presented an offset effect, which
showed a negative effect in hypertension and elevated
triglycerides. Further understanding of the contribution
of each individual component of MetS to changes in stroke
burden is important to help us more effectively identify
populations at increased risk of stroke recurrence. There
were a few limitations in this meta-analysis. One poten-
tial limitation of the present meta-analysis was the various
definitions of assessment for MetS used among studies.
Although the major components of these MetS defini-
tions are similar, individual components of MetS and their
diagnostic threshold values vary among different defi-
nitions. Thus, different diagnostic definitions of MetS may
lead to substantially different assessments even in the same
population. However, subgroup analyses by different def-
inition in our studies were not possible because of a lack
of data. A second limitation is we were unable to examine
95% CI I2 P for heterogeneity
1.12-2.47 .00% .8848
1.00-2.01 .00% .4325
METABOLIC SYNDROME AS PREDICTOR OF RECURRENT STROKE
the associations of the number of components with the
risk of cardiovascular disease because too few studies pro-
vided such detailed information. In order to inform for
the observed positive association between MetS and re-
current stroke risk, future research should comprise analyses
based on a standard definition of MetS and objective
biomarkers for assessing each MetS component. Further,
it would also be useful if future studies examined the
relationship between MetS and recurrent stroke risk sep-
arately in male and female because the gender differences
in the associations between MetS and the risk of cere-
brovascular diseases were observed in many previous
studies.24,25 In addition, adjustments for all important po-
tential confounders need to be made. Furthermore, they
need to be examined in ischemic stroke and cerebral hem-
orrhage separately in relation to MetS. In addition, large
and well-designed prospective studies are necessary to
further confirm the association between MetS and risk
for recurrent stroke in the future. In conclusion, the meta-
analysis suggests that MetS is an important predictor of
recurrent stroke. Moreover, our data provided useful in-
formation toward better understanding of individuals who
are at increased risk of stroke recurrence and the need
to develop preventive strategies directed to the control
of MetS and each of its component conditions for future
stroke.
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