ORIGINAL ARTICLE

EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

Effect of Bariatric Surgery on the Metabolic Syndrome:

A Population-Based, Long-term Controlled Study
JOHN A. BATSIS, MBBCH; ABEL ROMERO-CORRAL, MD, MSC; MARIA L. COLLAZO-CLAVELL, MD;
MICHAEL G. SARR, MD; VIREND K. SOMERS, MD, PHD; AND FRANCISCO LOPEZ-JIMENEZ, MD, MSC

OBJECTIVE: To assess the effect of weight loss by bariatric surgery

on the prevalence of the metabolic syndrome (MetS) and to
examine predictors of MetS resolution.
PATIENTS AND METHODS: We performed a population-based, retrospective study of patients evaluated for bariatric surgery between
January 1, 1990, and December 31, 2003, who had MetS as
defined by the American Heart Association/National Heart, Lung,
and Blood Institute (increased triglycerides, low high-density lipoprotein, increased blood pressure, increased fasting glucose, and
a measure of obesity). Of these patients, 180 underwent Roux-enY gastric bypass, and 157 were assessed in a weight-reduction
program but did not undergo surgery. We determined the change
in MetS prevalence and used logistic regression models to determine predictors of MetS resolution. Mean follow-up was 3.4
years.
RESULTS: In the surgical group, all MetS components improved,
and medication use decreased. Nonsurgical patients showed improvements in high-density lipoprotein cholesterol levels. After
bariatric surgery, the number of patients with MetS decreased
from 156 (87%) of 180 patients to 53 (29%); of the 157 nonsurgical patients, MetS prevalence decreased from 133 patients (85%)
to 117 (75%). A relative risk reduction of 0.59 (95% confidence
interval [CI], 0.48-0.67; P<.001) was observed in patients who
underwent bariatric surgery and had MetS at follow-up. The number needed to treat with surgery to resolve 1 case of MetS was
2.1. Results were similar after excluding patients with diabetes or
cardiovascular disease or after using diagnostic criteria other
than body mass index for MetS. Significant predictors of MetS
resolution included a 5% loss in excess weight (odds ratio, 1.26;
95% CI, 1.19-1.34; P<.001) and diabetes mellitus (odds ratio,
0.32; 95% CI, 0.15-0.68; P=.003).
CONCLUSION: Roux-en-Y gastric bypass induces considerable and
persistent improvement in MetS prevalence. Our results suggest
that reversibility of MetS depends more on the amount of excess
weight lost than on other parameters.

Mayo Clin Proc. 2008;83(8):897-906

ACEI = angiotensin-converting enzyme inhibitor; AHA = American Heart

Association; ARB = angiotensin receptor blocker; ATP = Adult Treatment Panel; BMI = body mass index; CI = confidence interval; CV =
cardiovascular; HDL-C = high-density lipoprotein cholesterol; MetS =
metabolic syndrome; NHLBI = National Heart, Lung, and Blood Institute; RYGB = Roux-en-Y gastric bypass; TG = triglyceride

he components of the metabolic syndrome (MetS) account for a substantial portion of the attributable risk
of atherosclerotic cardiovascular (CV) diseases. All 5 components of the American Heart Association (AHA)/National Heart, Lung, and Blood Institute (NHLBI) definition
of MetS have been linked independently to CV diseases,
Mayo Clin Proc.

including increased levels of serum triglycerides (TGs),

low levels of serum high-density lipoprotein cholesterol
(HDL-C), elevated blood pressure, increased fasting
plasma glucose levels, and an increased waist circumference.1 With the increasing prevalence of MetS and its
strong association with the development of diabetes mellitus and CV disease, this syndrome is an important public
health concern.2-4
Substantial evidence suggests that insulin resistance is
the underlying abnormality in the pathophysiology of
MetS5 and that lifestyle modifications are the cornerstone
of management.6,7 Increased physical activity and a healthy
diet for people with impaired fasting blood glucose reduces the incidence of type 2 diabetes mellitus,8 even
when weight loss is only modest (<10% of total body
weight).9 Because most dietary interventions do not
achieve more than a 10% weight loss and most lost weight
is regained, the net effect of considerable and long-lasting
weight loss on MetS is unknown.
Bariatric surgery, an approved treatment of obesity
when other measures have failed,10 induces long-standing,
profound weight loss.11 Most patients eligible for weight
reduction by bariatric procedures have a substantial number of components of MetS; most of their weight loss can
be attributed to reduced caloric intake and, to some extent,
partial malabsorption of nutrients or bypass of the duodenum by Roux-en-Y gastric bypass (RYGB). This patient
population presents a unique opportunity to determine the
effect of major weight loss on MetS prevalence without the

From the Division of Primary Care Internal Medicine (J.A.B.), Division of

Cardiovascular Diseases (A.R.-C., V.K.S., F.L.-J.), Division of Endocrinology,
Diabetes, Metabolism and Nutrition (M.L.C.-C.), and Department of Surgery
(M.G.S.), Mayo Clinic, Rochester, MN.
Dr Romero-Corral is supported by a postdoctoral fellowship from the American
Heart Association. Dr Somers is supported by grants from the National
Institutes of Health (HL-65176, HL-70302, HL-73211, and M01-RR00585).
Dr Lopez-Jimenez is a recipient of a Clinical Scientist Development Award from
the American Heart Association.
Presented in part at the 68th Annual Scientific Session of the American
Diabetes Association, San Francisco, CA, June 6-10, 2008 (Abstract #1747-P).
Individual reprints of this article are not available. Address correspondence to
Francisco Lopez-Jimenez, MD, MSc, Division of Cardiovascular Diseases,
Mayo Clinic, 200 First St SW, Rochester, MN 55905 (lopez@mayo.edu).
2008 Mayo Foundation for Medical Education and Research

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897

EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

confounding factor of increased (moderate to intense)

physical activity. We evaluated the effect of bariatric surgery on the prevalence of MetS in a population-based
cohort of patients with morbid class II to III obesity and a
body mass index (BMI) (calculated as weight in kilograms
divided by height in meters squared) of 35 or higher by
comparing the prevalence of MetS in patients who underwent RYGB and in nonsurgical patients.
PATIENTS AND METHODS
We performed a population-based, retrospective cohort
study of all Olmsted County, Minnesota, patients referred
for bariatric surgery at Mayo Clinics site in Rochester,
MN, between January 1, 1990, and December 31, 2003.
Patients were identified using a centralized diagnostic index and the Rochester Epidemiology Project. All bariatric
interventions in the county are performed at our institution.
The Rochester Epidemiology Project is a comprehensive
record-linkage system that has been funded continually by
the Federal government since 1966 for use in diseaserelated epidemiology.12 Olmsted County patients have all
their medical care indexed, allowing complete ascertainment of patients medical histories. The county is a relatively isolated and self-contained area. Medical care is
provided predominantly by Mayo Clinic and its hospitals
and by Olmsted Medical Center and its hospital. Health
care delivery by a limited number of private practitioners is
also captured. This study was approved by the institutional
review boards of Mayo Clinic and the Olmsted Medical
Center.
Patients primary place of residence was determined
using baseline demographic information, and county residence was verified using US Postal Service zip codes. The
surgical cohort was identified using the Mayo Surgical
Index, with weight reduction using RYGB as the primary
indication. Of the 231 Olmsted County residents who had
undergone RYGB, 16 patients were excluded because they
had a BMI less than 35, and 35 patients because they had
incomplete data or a follow-up of fewer than 3 months,
yielding a surgical cohort of 180 patients.
Our comparison group included patients who were
evaluated for bariatric surgery at the multidisciplinary
Mayo Clinic Nutrition Center but who did not undergo
surgery because they voluntarily declined it, were ineligible due to denial by insurance providers, or did not
maintain lifestyle interventions during their evaluation. A
minority were excluded for psychiatric reasons. As is often
the case in clinical practice, patient exclusion from bariatric
interventions was multifactorial. Of the 252 Olmsted
County patients who were identified, 19 were excluded
because they had a BMI less than 35 (most of whom under898

Mayo Clin Proc.

went revisional bariatric operative procedures for complications) and 76 because they had no further medical follow-up
or had a follow-up of less than 3 months. Our final comparison cohort consisted of 157 patients. Both surgical and
nonsurgical patients received medical and dietetic care as
well as extensive counseling about the importance of physical activity.
Time of bariatric surgery and time of nutrition consultation were considered the baseline time for the surgical and
nonsurgical groups, respectively. We defined our baseline
variables on the basis of information present in the medical
record from the baseline time or earlier; follow-up variables were based on information at time of last follow-up
evaluation. Because major weight loss or substantial metabolic changes do not typically occur before 3 months, all
patients in our study had a minimum follow-up of at least 3
months. Height and weight were measured in a standardized manner by a trained nurse. We used the method of
Robinson et al13 to calculate ideal body weight.
We diagnosed MetS using the 5 components described
by AHA/NHLBI in 20051: increased serum TG levels, low
serum HDL-C levels, increased blood pressure, increased
fasting plasma glucose, and increased waist circumference.
Because waist circumference was not documented routinely in the medical record, we used BMI as a surrogate for
central obesity; data have shown that most patients with a
BMI of 30 or higher have a large waist circumference.14
Patients who were taking fibrates or nicotinic acid or
whose serum TG levels were 150 mg/dL or higher were
classified as having hypertriglyceridemia. Serum HDL-C
levels were considered low if they were less than 40 mg/dL
in male patients and less than 50 mg/dL in female patients
or in patients treated with nicotinic acid or fibrates specifically for this disorder. We classified patients as having
hypertension if their blood pressure was higher than 135/85
mm Hg, or if they were taking any medications specifically
for hypertension, including -blockers, calcium channel
blockers, angiotensin-converting enzyme inhibitors (ACEIs),
angiotensin receptor blockers (ARBs), thiazides, or loop or
potassium-sparing diuretics. These medications were included only if the patient had a coexisting documented
diagnosis of hypertension. Increased fasting plasma glucose concentration was defined as greater than 100 mg/dL
without the diagnosis of diabetes mellitus. Patients were
considered to have diabetes mellitus if their fasting glucose
was 126 mg/dL or higher or if they were taking insulin or
oral hypoglycemic agents. A diagnosis of MetS required 3
or more criteria. Finally, we determined the effect on the
prevalence of MetS, defined as 2 or more components
without obesity as a diagnostic criterion. In a subanalysis of
surgical patients with a baseline diagnosis of MetS and
more than 1 year of follow-up, patients were classified as

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EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

MetS responders if they no longer fulfilled criteria for MetS

at their most recent evaluation and as nonresponders if they
continued to have 3 or more criteria of MetS at follow-up.
STATISTICAL ANALYSES
Continuous data are presented as mean SD and categorical data as number and percentage. Within-group comparisons between baseline and follow-up were compared using
a 2-sided, paired t test and Wilcoxon signed rank test for
continuous variables and a McNemar test for categorical
variables. Intergroup comparisons between surgical and
nonsurgical patients at baseline and changes between
groups were compared using a 2-sample t test of unequal
variances, a Wilcoxon rank sum test, a 2 test, or a Fisher
exact test, depending on the type of data. For changes in
categorical variables between groups, we compared the 3point scale distributions (improved, no change, worsened)
and applied the Cochran-Armitage trend test. We applied
logarithmic transformation because of the skewness of triglyceride values.
We sought to determine whether the amount of weight
loss, defined as the percent of excess weight lost, was the
main predictor of MetS resolution. We constructed multiple logistic regression models using backward selection
to identify predictors of MetS resolution at follow-up in
patients with MetS at baseline. Our inclusion threshold was
P<.25, and the exclusion threshold for variables was P=.10.
Initially, we excluded patients with a follow-up of less than
1 year because previous studies have suggested that weight
loss is not linear during this period11 and normally plateaus
after 1 year. The overall cohort of patients with MetS at
baseline was stratified by quartiles according to their follow-up time. Because of the limited number of events in
each group, we adjusted only for age and sex in these
multivariate analyses.
Models were created to test whether our primary predictor, percentage of excess weight lost, was significantly
different in these groups. We determined whether the
within-quartile coefficients differed within each cohort to
further elicit the effect of follow-up time. Because no differences were observed, we analyzed the entire cohort of
MetS patients at baseline with a follow-up greater than 1
year. Univariate predictors were then entered into a multivariate model, with the exception of any measures related to
weight or glucose, because of colinearity with percentage of
excess weight lost and diabetes, both predictors of interest.
The first model (Model 1) defined MetS as 3 or more
components. Because patients who undergo bariatric surgery lose weight and may be cured of their obesity, the
likelihood for MetS response is higher in these patients.
Therefore, to have a MetS definition independent of BMI,
we developed a second model (Model 2) defining MetS as
Mayo Clin Proc.

2 or more components and excluding obesity as a diagnostic criterion. This second model allowed us to determine
the potential role of percentage of excess weight lost on the
resolution of other components of MetS. We examined all
patients who had MetS at baseline, regardless of whether
they had undergone surgery; both models included
covariates, such as age, sex, baseline TG levels, presence of
diabetes at baseline, use of an ACEI or ARB, and percentage of excess weight lost. We separately adjusted for follow-up time as an additional covariate in a multiple logistic
regression analysis for MetS, defined as 3 or more components (Model 1A), and MetS, defined as 2 or more components (Model 1B), to ascertain whether this variable altered
our results.
We tested Model 1 solely on patients with baseline
MetS (3 components) who underwent bariatric surgery
and were followed up for more than 1 year to determine
possible associations with MetS resolution. The same
covariates as in the aforementioned models were included,
in addition to HDL-C levels. In the nonsurgical group, we
independently assessed percentage of excess weight lost as
a predictor in Models 1 and 2 and incorporated follow-up
time in Models 1A and 2A because we had little power to
detect the few MetS resolution outcomes for this particular
analysis. The strength of association between follow-up time
and percentage of excess weight lost was also determined
using a correlation coefficient.
SENSITIVITY ANALYSIS
Sensitivity analyses were performed on our data using a
carry-forward method of imputation for patients lost to
follow-up. Patients excluded from the analysis because of
missing data (bariatric group, 35 patients; nonsurgical
group, 76 patients) were assumed to have MetS both at
baseline and at follow-up when determining what the
within-group change in MetS prevalence would have been
using this approach. We also determined the effect of excluding patients who had a baseline diagnosis of both diabetes and CV disease (74 patients [41%] in the surgical
group and 56 [36%] in the nonsurgical group) and those
with only a diagnosis of diabetes (58 patients [32%] in the
surgical group and 40 patients [25%] in the nonsurgical
group). P<.05 was considered statistically significant. All
analyses were performed using JMP for SAS (Windows
version 7.0.0; SAS Institute, Cary, NC).
RESULTS
The baseline characteristics of the cohorts are shown in
Table 1. Patients who underwent bariatric surgery had a
higher BMI and were more likely to be taking insulin than
patients in the nonsurgical group, but they had a similar

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EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

TABLE 1. Baseline Characteristics of Olmsted County Residents

Evaluated for Roux-en-Y Gastric Bypassa,b

Age (y)
Female sex
Duration of follow-up (y)
Body mass index
Excess weight (kg)
Blood pressure (mm Hg)
Systolic
Diastolic
Serum biochemical
parameters (mg/dL)d
Total cholesterol
LDL-C
HDL-C
Triglycerides
Glucose
Creatinine
Diabetes
Ever smoker
Cardiovascular disease
Medications
Statins
-Blockers
Calcium channel blockers
ACEI/ARB
Diuretics
Insulin
Oral diabetes medications
MetS components
Obesity
Hypertriglyceridemia
Low HDL-C
Elevated blood pressure
Impaired fasting glucose

Surgical
(n=180)

Nonsurgical
(n=157)

P
valuec

4510
143 (79)
3.42.5
499
7824

4411
113 (72)
3.52.6
446
6317.3

.39
.11
.79
<.001
<.001

13416
8010

13418
7710

.79
.03

20039
11833
4511
190119
11838
1.00.2
58 (32)
25 (14)
29 (16)

20845
12236
4514
219155
12151
1.00.2
40 (25)
29 (18)
23 (15)

.08
.26
.65
.10e
.66
.32
.17
.25
.71

26 (14)
36 (20)
17 (9)
39 (22)
46 (26)
30 (17)
26 (14)
156 (87)
180 (100)
110 (61)
123 (68)
155 (86)
112 (62)

19 (12)
22 (14)
8 (5)
36 (23)
36 (23)
7 (4)
24 (15)
133 (85)
157 (100)
99 (63)
111 (71)
120 (76)
88 (56)

.53
.15
.13
.78
.58
<.001
.83
.61
>.99
.71
.64
.02
.25

ACEI = angiotensin-converting enzyme inhibitor; ARB = angiotensin

receptor blocker; HDL-C = high-density lipoprotein cholesterol;
LDL-C = low-density lipoprotein cholesterol; MetS = metabolic syndrome.
b
For continuous values, all values are represented as mean SD; for
categorical variables, values are represented as number (percentage) of
patients and are rounded to the nearest integer, unless otherwise indicated.
c
The 2-sample t test with unequal variances and the Wilcoxon rank sum
test were used for continuous data; the 2 test or Fisher exact test was
used for nonparametric data.
d
SI conversion factors: To convert cholesterol values (total, HDL-C,
LDL-C) to mmol/L, multiply by 0.0259; to convert triglyceride values
to mmol/L, multiply by 0.0113; to convert glucose values to mmol/L,
multiply by 0.0555; to convert creatinine values to mol/L, multiply by
88.4.
e
P value based on logarithmic transformation of triglycerides.

prevalence of MetS at baseline (156 patients [87%] vs 133

patients [85%]; P=.61) and a similar mean SD duration of
follow-up (3.42.5 vs 3.52.6 years; P=.79). Follow-up
ranged from 0.4 to 12.8 years for surgical patients (interquartile range, 1.4-4.4 years) and from 0.4 to 13.8 years for
nonsurgical patients (interquartile range, 1.5-5.0 years).
Follow-up was less than 1 year in 14 patients (8%) who
underwent surgery and in 15 patients (10%) who did not.
The correlation between duration of follow-up and percentage of excess weight lost was 0.14. A greater number of
900

Mayo Clin Proc.

patients in the surgical group than in the nonsurgical group

had 4 MetS components (76 patients [42%] vs 45 patients
[29%]; P=.001) (Figure 1).
SURGICAL GROUP
All MetS components improved at follow-up when measured as continuous or as categorical variables (Figure 2).
After bariatric surgery, the components with the greatest
decreases in prevalence were hypertriglyceridemia (42%,
from 110 to 35 patients), glucose intolerance/diabetes mellitus (39%, from 112 to 42 patients), and the obesity component (37%, from 180 to 114 patients). Mean lipid and
blood pressure values decreased despite a decrease in the
use of statins, diuretics, -blockers, and ACEIs (Table 2).
NONSURGICAL GROUP
Although systolic blood pressure and overall lipid values
improved in the nonsurgical group, the magnitude of improvement was far lower than in the bariatric surgery
group; a marked increase in the use of statins and antihypertensive agents was also noted for the nonsurgical group
at follow-up. The prevalence of MetS criteria other than
low HDL-C did not change. At follow-up, a greater number
of patients had type 2 diabetes mellitus and a greater proportion were taking insulin.
COMPARISON OF SURGICAL AND NONSURGICAL GROUPS
In both patients who underwent bariatric surgery and those
who did not, the overall prevalence of MetS decreased
significantly (Figure 2) (surgical group, 58% decrease [from
87% to 29%]; P<.001; nonsurgical group, 10% decrease
[from 85% to 75%]; P<.001). The absolute difference in
prevalence reduction between groups was 48% (95% confidence interval [CI], 38%-58%; P<.001), yielding a relative risk reduction with bariatric surgery of 0.59 (95% CI,
0.48-0.67; P<.001). The number of patients needed to treat
in order to cure 1 patient with MetS with bariatric surgery
was 2.1. This was based on all patients with MetS at
baseline, calculating the difference between the proportion
of nonsurgical patients with MetS at follow-up (82%) minus the proportion of surgical patients with MetS at followup (34%), divided by the control proportion (82%). The
mean number of components decreased from 3.7 to 1.9
(P<.001) in the bariatric surgery group and changed
slightly from 3.6 to 3.4 (P=.04) in the nonsurgical group.
Of the 157 nonsurgical patients, all met criteria for obesity
at baseline, and 155 patients (99%) remained obese at
follow-up. In the surgical group, all 180 patients met criteria for obesity at baseline, whereas only 114 (63%) were
obese at follow-up. After omitting BMI as a categorical
variable for MetS and defining MetS as 2 or more components, the prevalence in the surgical group decreased from

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EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

100

90

90

80

80

70

70

60

60

50

50

40

40

30

30

20

20

10

10

Prevalence (%)

100

No. of
MetS
components
5

0
Baseline

Follow-up

Baseline

Follow-up

Nonsurgical

Surgical

FIGURE 1. Baseline and follow-up prevalence of metabolic syndrome (MetS) components in surgical and nonsurgical patients.

158 patients (88%) to 67 patients (37%) (P<.001), whereas

in the nonsurgical group it decreased much less, from 138
patients (88%) to 117 patients (75%) (P<.001). Examination of our cohort, stratified by quartiles of follow-up time,
showed that the percentage of excess weight lost, as the
main predictor of MetS resolution, was highly significant
and did not change. Subsequently, performing multiple

100

logistic regression on the entire cohort of patients with

MetS at baseline showed that the percentage of excess
weight lost was the main predictor of MetS resolution
(Table 3). Again, results were no different after incorporating follow-up time as a covariate in the overall cohort after
adjusting for follow-up time (Model 1A and 2A). Separate
examination of the odds ratios of MetS resolution in the

100

90

90

80

*
80

Prevalence (%)

70

70

*
*

60

60

50

50

40

40

30

30

20

20

10

10
0

0
Obesity

TG

HDL-C

HTN

Glucose

MetS

Obesity

Surgical

TG

HDL-C

HTN

Glucose MetS

Nonsurgical

FIGURE 2. Change in the prevalence and in each of the 5 components of the metabolic syndrome as defined by the American Heart
Association/National Heart, Lung, and Blood Institute. Dark bars represent baseline prevalence, and lighter bars represent
prevalence at follow-up. Significant changes (P<.05) are represented by an asterisk. HDL-C = high-density lipoprotein cholesterol;
HTN = hypertension; MetS = metabolic syndrome; TG = triglycerides.

Mayo Clin Proc.

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EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

TABLE 2. Change in Parameters from Baseline to Follow-up

in Olmsted County Residents Referred for Roux-en-Y
Gastric Bypassa,b

Age (y)
Body mass index
Excess weight (kg)
Excess weight lost (%)
Blood pressure, mm Hg
Systolic
Diastolic
Serum biochemical
parameters (mg/dL)d
Total cholesterol
LDL-C
HDL-C
Triglycerides
Glucose
Creatinine
Diabetes (%)
Cardiovascular disease (%)
Medications
Statins
-Blockers
Calcium channel blockers
ACEIs/ARBs
Diuretics
Insulin
Oral diabetes medications

Surgical
(n=180)

Nonsurgical
(n=157)

P
valuec

3.42.5
166
4417
5920

3.52.6
0.16.0
0.316
0.229

.74
<.001
<.001
<.001

1318
813

621
213

<.001
<.001

4639
4134
911
80103
2434
0.050.15
37 (21)
4 (2)

1543
1334
411
44112
447
00.15
14 (9)
6 (4)

<.001
<.001
<.001
.001
<.001
.02
<.001
.39

31 (20)
11 (7)
1 (1)
21 (13)
17 (11)
12 (8)
14 (9)

<.001
<.001
.75
<.001
<.001
<.001
.29

14 (7)
15 (8)
1 (1)
9 (5)
17 (9)
24 (13)
24 (13)

ACEI = angiotensin-converting enzyme inhibitor; ARB = angiotensin

receptor blocker; HDL-C = high-density lipoprotein cholesterol; LDL-C =
low-density lipoprotein cholesterol.
b
Values are mean difference SD for continuous variables. Differences
in each cohort represent ValueFOLLOW-UP ValueBASELINE. For categorical
values, the change in the number of patients (Follow-up Baseline)
renormalized to the baseline number of patients in each cohort is represented (percentage) and is rounded to the nearest integer, unless otherwise indicated. A negative value represents an improvement in the variable for continuous data and a reduction in the net number (% reduction)
of patients for categorical data.
c
The 2-sample t test for unequal variances and the Wilcoxon rank sum
test were used to test the differences between continuous data for surgical and nonsurgical patients; the Cochran-Armitage trend test was used
for categorical variables.
d
SI conversion factors: To convert cholesterol (total, HDL-C, LDL-C)
values to mmol/L, multiply by 0.0259; to convert triglyceride values to
mmol/L, multiply by 0.0113; to convert glucose values to mmol/L,
multiply by 0.0555; and to convert creatinine values to mol/L, multiply
by 88.4.

surgical group (Table 3) and nonsurgical group (data not

shown) for percentage of excess weight lost as our primary
predictor revealed no differences between these values after adjustment for follow-up time. All the above analyses
suggest that follow-up time was not a significant contributor to MetS resolution.
SURGICAL METS RESPONDERS VS METS NONRESPONDERS
Of the 156 patients who underwent bariatric surgery and
had MetS at baseline, 13 (8%) with a follow-up of less than
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Mayo Clin Proc.

1 year were excluded for this particular analysis. Of the

remaining 143 patients (79%) with a baseline diagnosis of
MetS, 45 patients (31%) did not have resolution of their
MetS during follow-up and were considered MetS nonresponders. The mean number of components decreased
from 3.9 to 1.3 (P<.001) in the MetS responders and from
4.2 to 3.5 (P<.001) in the MetS nonresponders. The number of MetS responders fulfilling the obesity criterion decreased from 98 patients (100%) to 51 patients (52%)
(P<.001), whereas the number of MetS nonresponders fulfilling the obesity criterion decreased from 45 patients
(100%) to 40 (89%) (P=.02). These MetS nonresponders
were older and had a higher baseline BMI, a lower percentage of excess weight lost, higher serum levels of TGs,
higher fasting blood glucose concentrations, a greater
prevalence of baseline diabetes mellitus, and increased use
of ACEIs or ARBs (Table 4). No differences in the individual components of MetS at baseline were observed.
Percentage of excess weight lost was a highly significant
predictor of MetS resolution, even after adjusting for follow-up time (Table 3).
SENSITIVITY ANALYSIS
Our sensitivity analysis, which assumed that patients with
missing data would not have MetS resolution at follow-up,
showed a 49% reduction in MetS prevalence in the 215
patients in the bariatric cohort, from 194 (90%) to 88
patients (41%) vs a 7% reduction in MetS prevalence in the
233 patients in the nonsurgical group, from 209 (90%) to
193 patients (83%). In another sensitivity analysis, after
excluding patients with a baseline diagnosis of both diabetes mellitus and CV disease, no differences in baseline
prevalence of MetS (P>.99) were observed. Of the 101
nonsurgical patients, 79 (78%) had MetS at baseline and 66
(65%) at follow-up (P=.02). In the surgical cohort, of the
106 patients without baseline diabetes or CV disease, 83
(78%) had MetS at baseline compared with 19 (18%) at
follow-up (P<.001). Results were similar after exclusion of
patients with baseline diabetes mellitus.
DISCUSSION
Our population-based study shows that MetS is a largely
reversible phenomenon in patients with class II to III
obesity and that reversibility of MetS depends more on the
percentage of excess weight lost than on other clinical or
demographic characteristics. Although the reversibility
could be influenced by or associated with factors such as
age, baseline serum TG levels, and baseline diabetes status,
these factors, although significant in our univariate analysis at follow-up, were not as strongly predictive for MetS
resolution as percentage of excess weight lost. This asso-

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EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

TABLE 3. Multivariate Logistic Regression Models Identifying Predictors of MetS Resolution

in Patients With a Follow-up Greater Than 1 Year a,b

Age
Male sex
Triglycerides
Diabetes (yes/no)
ACEI/ARB
HDL-C
% EWLd
5% change in % EWL
Follow-up time

Surgical responders vs nonresponders

with MetS at baseline
Model 1
Model 1Ac

Model 1
P
OR
value

Overall cohort with MetS at baseline

Model 2
Model 1Ac
P
P
OR
value
OR
value

OR

P
value

OR

P
value

OR

P
value

0.94
1.07
0.28
0.32
0.40
NA
1.05
1.26
NA

0.94
1.09
0.28
0.32
0.40
NA
1.05
1.26
0.98

0.95
0.85
0.35
0.26
0.55
NA
1.03
1.18
1.03

.003
.66
.002
<.001
.11
NA
<.001
<.001
.65

0.93
1.24
0.33
0.41
0.34
1.02
1.05
1.28
NA

.009
.71
.03
.06
.03
.37
<.001
<.001
NA

0.93
1.23
0.33
0.41
0.34
1.02
1.05
1.28
1.01

.009
.73
.03
.06
.03
.38
<.001
<.001
.92

.001
.86
.001
.003
.02
NA
<.001
<.001
NA

.001
.83
.001
.003
.02
NA
<.001
<.001
.75

0.95
0.87
0.35
0.26
0.54
NA
1.03
1.17
NA

.003
.69
.002
<.001
.11
NA
<.001
<.001
NA

Model 2Ac

ACEI = angiotensin-converting enzyme inhibitor; ARB = angiotensin receptor blocker; EWL = excess weight lost; HDL-C = high-density lipoprotein
cholesterol; MetS = metabolic syndrome; NA = not applicable; OR = odds ratio.
Separate models were constructed for the overall cohort consisting of both surgical and nonsurgical patients with MetS at baseline and for patients
undergoing bariatric surgery who had MetS at baseline. All patients had a follow-up of greater than 1 year. MetS was defined as 3 or more of 5 components
of American Heart Association/National Heart, Lung, and Blood Institutedefined MetS in Model 1. Model 2 consists of 2 or more of 4 components
(excluding the obesity component). Covariates in the overall cohort for Models 1 and 2 were age, sex, baseline serum triglyceride levels, presence of
diabetes mellitus at baseline (yes/no), use of ACEIs or ARBs at baseline (yes/no), and percentage of EWL. For the surgical cohort alone (MetS responders
and MetS nonresponders), HDL-C was added as a covariate in the multivariate analysis for Model 1. Follow-up time was included as a covariate in the
multiple logistic regression models labeled with the suffix A.
c
Models including time as a covariate.
d
Per 1% unit change in excess weight lost.
b

ciation persisted even in the BMI-independent definition of

MetS, suggesting its importance in relation to the other
MetS components. Patients in the structured, multidisciplinary, nonsurgical program showed minimal weight
changes associated with improvements in systolic blood
pressure and lipid parameters; however, many of these
improvements may have been related to more aggressive
pharmacotherapy, given that a considerably greater number of nonsurgical patients were taking statins or antihypertensive agents at follow-up.
Relatively few studies have used established MetS criteria in evaluating outcomes after bariatric surgery.15,16 All
confirm our results, showing marked reductions in the
prevalence of MetS and in the number of MetS components. Several studies have examined non-American populations,16-19 in whom RYGB often is not used. Of studies
performed in the United States with RYGB, Madan et al20
showed a decrease in MetS as defined by Adult Treatment
Panel (ATP) III from 78% to 2%; however, this study was
relatively small, did not have a nonsurgical group, and had
a limited follow-up of 1 year. A study by Mattar et al21
found a decrease from 70% to 14% in a series of 70 patients. Although their follow-up was somewhat longer,
their study had limitations similar to those of the Madan
study. Morinigo et al22 examined RYGB using criteria from
the ATP III, showing a decrease in MetS prevalence from
55% to 36% at 6 weeks and to 11% at 52 weeks, but their
study was limited to 36 patients with no control group. Our
Mayo Clin Proc.

study confirms and expands these findings with the use of

state-of-the-art epidemiologic methods supporting these
conclusions.
To our knowledge, our study is the first to assess predictors of MetS resolution in patients with class II to III
obesity, showing that percentage of excess weight lost is
the main predictor of whether a patient will be cured of
MetS at follow-up. The use of an obesity-independent definition of MetS confirmed the importance of excess weight
lost on resolution of MetS. Our study provides robust data
to practicing clinicians about the benefits of counseling
weight reduction in MetS patients.
Our results have important clinical implications because
they further our understanding of the possible reversibility
of MetS with weight loss. Does this reduction in MetS
prevalence after bariatric surgery, and specifically after
RYGB, reduce CV disease? No studies have used riskprediction functions in patients with MetS after bariatric
surgery. However, in the past year, several studies 23,24 have
projected significant reductions in CV risk and death, including our own study that used risk modeling derived
from the National Health and Nutrition Examination Survey and applied it to this specific cohort,25 estimating that 4
overall deaths and 16 CV events would be prevented by
bariatric surgery per 100 patients at 10 years. The few
studies that have examined specifically the decrease of
actual CV events and overall mortality likely underestimate the value of bariatric surgery because of lack of

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903

EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

TABLE 4. Baseline Characteristics of 143 Roux-en-Y Gastric

Bypass Patients With MetS at Baseline, Stratified by
MetS Responders vs Nonresponders
With a Follow-up of Greater Than 1 Yeara,b,c

Responders
(n=98)
Age (y)
Female sex (%)
Body mass index
Excess weight (kg)
Excess weight lost (%)
Blood pressure (mm Hg)
Systolic
Diastolic
Serum biochemical
parameters (mg/dL)e
Total cholesterol
LDL-C
HDL-C
Triglycerides
Glucose
Creatinine
Diabetes (%)
Ever smoker (%)
Cardiovascular
disease (%)
Medications
Statins
-Blockers
Calcium channel
blockers
ACEI/ARB
Diuretics
Insulin
Oral diabetes
medications
MetS component
Obesity
Hypertriglyceridemia
Low HDL-C
Elevated blood
pressure
Impaired fasting
glucose

MetS
Nonresponders
(n=45)

4310
77 (79)
498
7624
6320

4810
35 (78)
5211
8225
4918

P
valued
.009
.91
.05
.20
<.001

13416
8010

13516
7911

.82
.74

19941
11933
449
17788
11838
1 0.2
28 (29)
18 (18)

19937
11028
4111
254169
13340
10.2
28 (62)
5 (11)

.62
.12
.07
<.001
.03
.71
<.001
.27

15 (15)

9 (20)

.49

16 (16)
19 (19)

7 (16)
12 (27)

.91
.33

10 (10)
15 (15)
26 (27)
16 (16)

6 (13)
16 (36)
14 (31)
10 (22)

.58
.006
.57
.40

13 (13)

7 (16)

.71

98 (100)
65 (66)
72 (73)

45 (100)
34 (76)
37 (82)

>.99
.27
.25

85 (87)

41 (91)

.45

65 (66)

36 (80)

.10

ACEI = angiotensin-converting enzyme inhibitor; ARB = angiotensin

receptor blocker; HDL-C = high-density lipoprotein cholesterol; LDLC = low-density lipoprotein cholesterol; MetS = metabolic syndrome.
b
Responders are defined as patients undergoing Roux-en-Y gastric bypass who have MetS at baseline and are cured of MetS at follow-up.
c
All variables are mean SD for continuous variables or number (percentage) of patients for categorical variables and are rounded to the
nearest integer, unless otherwise indicated.
d
The 2-sample t test with unequal variances and Wilcoxon rank sum test
were used for continuous data; the 2 test or Fisher exact test was used
for categorical data. P values are testing the differences in baseline
parameters between MetS responders and MetS nonresponders.
e
SI conversion factors: To convert cholesterol values (total, HDL-C, LDL-C)
to mmol/L, multiply by 0.0259; to convert triglyceride values to mmol/L,
multiply by 0.0113; to convert glucose values to mmol/L, multiply by
0.0555; and to convert creatinine values to mol/L, multiply by 88.4.

follow-up information or use of hospital controls.26-28 Recently, 2 studies have confirmed our previously published
estimated risk reduction after bariatric surgery.29,30 One
904

Mayo Clin Proc.

study of 9949 patients who had undergone RYGB showed

a 40% survival benefit for them compared with obese
control patients;29 cause-specific mortality due to coronary artery disease was reduced by 56%. Furthermore, the
Swedish Obesity Study showed a risk reduction of 29% at
10 years.30 Mortality rates could decrease after bariatric
surgery in part because of the total or partial resolution of
MetS.
Bariatric surgery decreases fat stores31 and offers an
opportunity to better understand the reversibility of MetS
with profound weight loss. Weight loss is known to reduce blood leptin and ghrelin levels, increase adiponectin
levels, improve insulin sensitivity, and reduce fatty acid
turnover; it is also associated with a decrease in systemic
inflammation and improved endothelial function.32 Further investigation is needed to determine whether incretin
levels, insulin sensitivity, and glucose intolerance are affected differently by a duodenal bypass procedure vs gastric banding.
The main strength of our study is its use of the Rochester Epidemiology Project to ascertain the outcomes of all
patients referred for RYGB in Olmsted County, Minnesota. By using a population-based cohort, we minimized
the selection and referral bias often observed at tertiary
care institutions performing this surgery. Previous studies
have shown reasonable extrapolation of data to other
parts of the United States using this population.12 The
ability to abstract a patients entire medical record ensured that all information and outcomes relevant to this
study were available. Although a few studies have examined the effect of bariatric surgery in patients with MetS,
none have had a nonsurgical group whose characteristics
were similar to surgical patients, and many have been
performed in Europe, where alternative techniques, including biliopancreatic bypass and gastroplasty, are used.
No recent studies have used the most updated MetS criteria published by the AHA/NHLBI. Most studies of MetS
parameters after RYGB examine outcomes up to 1 year,
whereas our study provided follow-up of more than
3 years. The use of an obesity-independent definition also
lends credence to our results. The sensitivity analysis
we performed to determine the effect of missing patients on our intragroup results ensures that, in a worst
case scenario in which these missing patients had no
metabolic improvements, the effect on our study results
would be minimal, allowing adequate generalization of
these results.
As with any retrospective study, recording and measurement bias are inherent issues in the study design. We had
no control over when patients had their laboratory or clinical assessment. Information was unavailable regarding
known confounders, such as exercise, dietary habits, diag-

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EFFECT OF BARIATRIC SURGERY ON THE METABOLIC SYNDROME

nosis or management of obstructive sleep apnea, and leptin

or insulin sensitivity. However, these issues would be
present in both groups and at both points in time. The
variability in the follow-up time created inherent challenges in analyzing our data. As a rule, Cox proportional
hazards models should be used in inception cohorts in
which time to last follow-up is variable, patients are exposed to the predictor of interest from the beginning of the
follow-up, the risk is proportional to the time of follow-up,
and the timing of the outcome is well known. In our study
group, none of the last 3 assumptions were met. Weight
loss, particularly with bariatric surgery, usually occurs in a
nonlinear fashion within the first year,11 and subsequent
weight regain is minimal. However, once it was shown that
the length of follow-up did not affect the association between percentage of excess weight lost and the resolution
of MetS, logistic regression appeared to be more appropriate than the Cox proportional hazards model. Acknowledging the limitations of both approaches, we attempted to
prove that percentage of excess weight lost remained significant in each of these analyses by eliminating patients
with less than 1 year of follow-up and stratifying the remaining cohort by follow-up time. Adjusting our models
by follow-up time also confirmed these results. This approach suggests that percentage of excess weight lost remains the main predictor of MetS resolution at 1-year
follow-up.
The decision to undergo bariatric surgery cannot be
allocated randomly. We made no attempt to match our
nonsurgical group to our bariatric surgery group. Ideally, in
a matched analysis we would have required a greater number of nonsurgical patients, which was not possible in this
retrospective study. In addition, our nonsurgical group
should not be considered a true control group but instead a
population-based cohort of patients referred for surgical
intervention who did not undergo operative treatment.
Therefore, our results may not be generalizable to all
patients attempting weight loss with nonsurgical approaches. Furthermore, very few of the nonsurgical patients achieved a weight loss that exceeded the mean
weight loss of the surgical group, suggesting that our
results would not be significantly affected if we eliminated specific groups of patients, such as the
underinsured. Our findings can be applied only to patients
with class II to III obesity who have undergone evaluation
for RYGB bariatric surgerythe patient population that
is most eligible for bariatric procedures10and hence
cannot be extrapolated to nonobese patients with MetS or
to patients treated with other types of bariatric procedures, including gastric banding.
Although MetS is thought to lead to the development of
both type 2 diabetes mellitus and CV disease, we included
Mayo Clin Proc.

patients with both these diagnoses. One of the primary

controversies in the MetS literature is the inclusion of
diabetes mellitus in ATP definition criteria. Our study
showed that results were not altered after excluding patients with preexisting diabetes mellitus or CV disease at
baseline in our sensitivity analysis.
CONCLUSION
Bariatric surgery is an effective means of reversing or
controlling MetS in patients eligible for surgically induced
weight loss. This current study provides strong evidence
that percentage of excess weight lost after RYGB is a
primary contributor to reduced MetS prevalence and is
independent of the obesity component. We suggest that
RYGB should be considered as a treatment option in patients with MetS that has not responded to conservative
measures.

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