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Diabetes Care Volume 39, Supplement 2, August 2016
OBESITY
S268
Revisiting the Role of BMI in the
Guidelines for Bariatric Surgery
Gabriella Segal-Lieberman,1
Pesach Segal,2 and Dror Dicker3
Diabetes Care 2016;39(Suppl. 2):S268–S273 | DOI: 10.2337/dcS15-3018
The high and growing prevalence of obesity worldwide, combined with the corresponding increase in the prevalence of diabetes, and further combined with the
relatively poor long-term success of conservative obesity treatment, led to a sharp
escalation in the use of bariatric surgery, the prevalence of which has tripled in the
past decade (1). A total of 468,609 bariatric procedures were performed worldwide in the year 2013 according to the International Federation for the Surgery of
Obesity and Metabolic Disorders (IFSO) survey (1), and this extraordinary acceptance, by both patients and physicians, stems from the fact that these procedures
are not only efficient for weight loss but also effective in treating the metabolic
syndrome in people with obesity. Bariatric surgery, as its name suggests, was
originally designed to reduce weight, with current eligibility criteria being BMI
$40 or $35 kg/m2 with comorbidities, while lower BMIs are excluded. However,
its significant beneficial impact on several components of the metabolic syndrome, particularly uncontrolled diabetes, led to the introduction of bariatric
surgery as a means to treat diabetes two to three decades ago (2–4), yet only in
obese individuals. Since then, along with the improvement in surgical technique,
bariatric surgery performed in morbidly obese individuals established itself not
only as the most effective means of treating diabetes but also as a “cure” to the
disease in a significant proportion of the cases (5–7). The excellent results of
bariatric surgery in improving glucose homeostasis in obese patients with type 2
diabetes led to the coinage of the term “metabolic surgery” (8), wherein amelioration of hyperglycemia in obese patients with type 2 diabetes has been observed
even before a significant weight loss has taken place (9). Several mechanisms were
offered to explain this dramatic impact of bariatric surgery on glucose homeostasis
in patients with diabetes, including changes in the secretion of glucagon-like
peptide 1, fibroblast growth factor 19, and bile acid as well as in the gut microbiota
(10–13). Although the exact mechanisms that lead to postsurgical remission of
type 2 diabetes are not fully understood, the fact that the metabolic improvement
seems to be, at least partially, weight loss independent provides sufficient basis to
consider “bariatric” surgery for nonmorbidly obese or even nonobese metabolically impaired patients.
Before we enter a debate over bariatric surgery as a treatment for the metabolic
syndrome, especially uncontrolled diabetes, in less obese individuals, it is important
to review the factual and observational insights stemming from two decades of
accumulating experience.
In a large meta-analysis summarizing 621 studies with morbidly obese patients
with diabetes undergoing bariatric surgery, a dramatic impact of surgery on diabetes outcomes with an average 2.1% decrease in HbA1c and a diabetes remission rate
of 78.1% has been found (14). However, this work is based on cohorts lacking a longterm follow-up period. In trials where the follow-up period is extended to $5 years,
diabetes remission rate is lower, and a significant percent of the patients in remission eventually relapse (15–17). The Swedish Obese Subjects (SOS) study, providing
15 years of follow-up (17), has shown a high rate of diabetes relapse after an initial
remission (occurring in .50% of the patients) and has also shown that the impact of
bariatric surgery on long-term diabetes remission is reserved for patients with a short
duration of disease. However, both microvascular and macrovascular complications in
this cohort were significantly lower in operated patients compared with the control
group, suggesting that the benefits of bariatric surgery may encompass important
advantages beyond diabetes remission.
1
Institute of Endocrinology, Sheba Medical
Center, Ramat Gan, Israel
Sackler Faculty of Medicine, Tel Aviv University,
Tel Aviv, Israel
3
Internal Medicine D and Obesity Clinic,
Hasharon Hospital, Rabin Medical Center,
Sackler Faculty of Medicine, Tel Aviv University,
Tel Aviv, Israel
2
Corresponding author: Gabriella Segal-Lieberman,
[email protected].
This publication is based on the presentations
at the 5th World Congress on Controversies to
Consensus in Diabetes, Obesity and Hypertension (CODHy). The Congress and the publication
of this supplement were made possible in
part by unrestricted educational grants from
AstraZeneca.
© 2016 by the American Diabetes Association.
Readers may use this article as long as the work is
properly cited, the use is educational and not for
profit, and the work is not altered.
care.diabetesjournals.org
Wentworth (26)
Navarrete (72)
DePaula (25)
First author
(reference no.)
RYGB or MGB
Gastric banding
SG + DJB
IIP + SG
Type of surgery
103
25
10
69
N
,30
25–30
,30
21–29
BMI (kg/m2)
12
24
12
21
Follow-up
time (months)
9.1
6.9
9
8.7
Baseline
HbA1c (%)
6.9
6.8
6.1
6.3
5.9
Final
HbA1c (%)
27
30
52
40
65
Diabetes
remission rate (%)
HbA1c #6%
FPG ,126 + PPG ,200
HbA1c ,7%
HbA1c ,6%
Diabetes
remission definition
NR
TG↓
TC↓, TG↓
TG↓, LDL-C↓
Change in
lipid profile
NR
No
NR
Yes
Decrease in
blood pressure
Table 1—Metabolic changes after bariatric surgery in nonobese subjects with diabetes
Dixon (27)
9.1
6.8
24
9.1
25–29.9
12
15
,30
BPD
Scopinaro (28)
80
HbA1c #6% + FPG #125
RYGB, SG, or MGB
25
HbA1c #6%
TG↓, HDL-C↑
TG↑↑, HDL-C↓
Yes
Yes
Several studies have attempted to evaluate the effect of bariatric surgery on metabolic syndrome in patients with stage 1
obesity (BMI 30–35 kg/m2) and in the
nonobese population (BMI ,30 kg/m2).
Studies in which Roux-en-Y gastric bypass (RYGB) was performed in patients
with diabetes with stage 1 obesity
show a significant, albeit inconsistent, diabetes remission rate ranging from 25 to
88% in similar populations (5,18). This
ability to surgically cure diabetes declines even further where nonobese patients with diabetes are concerned.
While a large meta-analysis on bariatric
surgery performed in morbidly obese patients with diabetes shows an average
decrease in HbA1c of 2.1% and a diabetes
remission rate of 78.1% (14), a smaller
meta-analysis, looking at 290 patients
with diabetes with a BMI ,30 kg/m2, is
much less impressive, with an average
decrease in HbA1c of 1.88% and a remission rate of only 42% (19). However, it
should be noted that these two metaanalyses entailing different procedures,
with diverse definitions of remission, are
hard to compare.
Only a small number of studies have
been directed to the outcome of metabolic surgeries in the nonobese population. These studies were performed
mostly on small cohorts of patients with
uncontrolled diabetes, using diverse surgical techniques and allowing a relatively
short follow-up period, with inconsistent
Lee (29)
Bariatric Surgery Should Be
Performed Only in Obese Individuals
results (20–24). Studies with a follow-up
period of at least 12 months are summarized in Table 1.
An ileal interposition was performed
along with a diverted sleeve gastrectomy
in 69 patients with diabetes with a BMI
of 21–29 kg/m2 (25). In this cohort, average HbA1c decreased from 8.7 to 5.9%,
with 65% of the cohort achieving “remission” of diabetes after an average 21month follow-up perioddmarginally
lower than the remission rate seen in
the obese population. An Australian
randomized study using the gastric
banding operation versus medical
treatment in overweight patients with
diabetes (BMI 25–30 kg/m2) showed a
diabetes remission rate of 52% in the
surgical group compared with 8% in the
medical group after 2 years of followup (26). RYGB or a mini–gastric bypass,
performed in 103 patients with uncontrolled diabetes with an average BMI
of 26 kg/m 2, resulted in a somewhat
lower remission rate of only 30%
after a 12-month follow-up period
(27). A 2-year follow-up after a biliopancreatic diversion (BPD) procedure
performed in 15 nonobese (BMI 25–
30 kg/m 2 ) and 15 obese (BMI 30–
35 kg/ m 2 ) subjects with diabetes
revealed a vast difference in diabetes remission rate between the two groups,
reaching 27 and 67% in the nonobese
and obese groups, respectively (28);
this observation suggests that diabetes
occurring at a lower BMI is more resistant to bariatric treatment. A metabolic
surgery was performed in 80 nonobese
and 432 obese (BMI .30 kg/m2) subjects
with diabetes in a single medical institution in Taiwan (29). In this study, the
diabetes remission rate observed in
the nonobese group was 25%, which
was significantly lower than the remission rate observed in subjects with a
higher BMI (49.5 and 79% in subjects
with a BMI of 30–35 and .35 kg/m2,
respectively).
Taken together, studies performed in
subjects with diabetes with lower BMIs
undergoing bariatric surgery demonstrate that these procedures are much
less effective in these patients and raise
the question: why do patients with diabetes with a lower BMI react differently to surgery?
Type 2 diabetes is a heterogeneous
group of diseases, with diverse degrees
of insulin sensitivity and b-cell function.
Fasting plasma glucose (FPG) and plasma glucose after 75-g oral glucose (PPG) measured in mg/dL. DJB, duodenojejunal bypass; HDL-C, HDL cholesterol; IIP, ileal interposition; LDL-C, LDL cholesterol, MGB,
mini–gastric bypass; NR, not reported; SG, sleeve gastrectomy; TC, total cholesterol; TG, triglycerides.
Hence, it is safe to say at this point in
time that bariatric surgery in eligible patients improves diabetes control and
seems to improve both micro- and macrovascular disease, whereas long-term
remission, or “cure” of diabetes, is only
partial and temporary.
What happens when bariatric surgery
is performed in “noneligible” patients,
who are leaner than prescribed by
guidelines? Are the metabolic advantages of the procedure outlined above
still present in the nonobese population? Does an obese patient with diabetes suffer from the same disease as a
lean patient with diabetes? Is it justified,
at this point in time, to overlook BMI as
the major determinant in deciding
which patient to operate? Or should
metabolic surgery still be reserved only
for obese individuals?
Segal-Lieberman, Segal, and Dicker
S269
S270
BMI as a Criteria for Bariatric Surgery
Subtypes of type 2 diabetes include
conditions such as ketosis-resistant diabetes of the young, a lean type 2 diabetes variant, and the like. Lean type 2
diabetes is not a rare condition in Western society; in a study in a large Chicago
cohort, comprising 18,000 subjects with
diabetes, 13% had a BMI of #25 kg/m2
(30). This study compared 1,784 normalweight patients with diabetes (average
BMI 23 kg/m2 ) with 8,630 obese patients with diabetes (average BMI
35.6 kg/m2) and found that nonobese
diabetes is more prevalent in men
and that subjects have a higher insulinuse rate and a lower triglycerideto-HDL ratio, suggesting a state of
increased b-cell failure as opposed to
insulin resistance, the latter being more
prevalent in subjects with diabetes
with a higher BMI. Furthermore, genetic
predispositions, affecting insulin secretion, may also contribute to diabetes occurring at a relatively low BMI (31).
These observations provide additional
evidence suggesting that nonobese individuals with type 2 diabetes represent a
unique subgroup that does not respond
to metabolic surgery as robustly as does
the obese population with diabetes.
Other aspects of the metabolic syndrome that seem to be less affected
by surgery in the nonobese population
should also be considered. A metaanalysis on nonobese patients with diabetes undergoing metabolic surgery
showed that hypertension had been resolved in 89% of the subjects; however,
total cholesterol and triglyceride levels
were not significantly changed after surgery (19). Interestingly, one of the articles included in this study reported
an unexpected increase in triglyceride
levels, which was still detected 2 years
after a BPD operation (28). Although this
unfavorable outcome in terms of triglycerides and HDL is based on a small population and may be related specifically to
the BPD operation, there is no evidence
that bariatric surgery in nonobese subjects improves lipid profile. This outcome
should be considered by practitioners referring patients to surgery in an attempt
to improve lipid profile.
Cardiovascular events and survival
rate, which are affected by bariatric procedures, now enter the equation. Studies underlying the increased survival and
decreased cardiovascular event rates after bariatric surgery are not randomized
Diabetes Care Volume 39, Supplement 2, August 2016
and were all performed on morbidly
obese individuals (32–36). To date, there
is no substantiating evidence based on
randomized controlled studies that bariatric
surgery has a beneficial impact on hard
end points such as mortality and/or
cardiovascular events in obese subjects,
let alone in nonobese subjects.
Bone density is yet another aspect
that has to be taken into consideration.
Several studies looking at bone metabolism after bariatric surgery have shown
that surgery may induce a significant
amount of bone loss (37–40). There
are several explanations for decrease
in bone mass, which include the reduction of mechanical load on the skeleton,
secondary hyperparathyroidism due to
reduced absorption of calcium and/or
vitamin D, and changes in gut peptides
(40–42). It stands to reason that nonobese individuals, not sharing the same extent of mechanical load protection as
obese individuals, will be more prone
to bone loss, especially after malabsorptive procedures, which are relatively
prevalent as metabolic surgeries.
One of the most vital factors affected
by bariatric surgery is quality of life
(QOL). Both obesity-related and diseaserelated QOL seem to improve after
bariatric procedures in obese individuals
(43). This comes as no surprise, since
for a morbidly obese individual, losing a
significant amount of weight may be a
life-changing event. However, obesityrelated QOL is irrelevant to the nonobese
population, whereas metabolic diseases
are only partially resolved in this population. Only limited data pertaining to QOL
are available for the nonobese population, with one study demonstrating an
improvement in physical (but not mental)
well-being after gastric banding (26).
Finally, complication rate is a major
consideration and is relatively high
in nonobese metabolic surgery compared with bariatric surgery. In an
above-mentioned meta-analysis, a 6.2%
major surgical complication rate, including intestinal obstruction, intestinal perforation, and intra-abdominal bleeding,
was reported, as well as a 1.7% reoperation rate (19). This rate is much higher
than the 3.2% complication rate reported
in patients with a somewhat higher
BMI (44).
In summary, studies performed in
nonobese subjects with diabetes undergoing bariatric surgery, compared with
the same in obese subjects, reveal that
surgery in this population is less effective as a means to control both diabetes
and dyslipidemia, its ability to reduce
cardiovascular disease as well as reduce
mortality rate is a mere speculation, it
may entail an increased risk of bone loss,
and it involves a notable increase in the
rate of complications. Even the wellappreciated improvement in QOL seen
in morbidly obese individuals who undergo surgery does not seem to be as
impressive where nonobese individuals
are concerned. Given the above, it is apparent that bariatric surgery should not
be routinely recommended in nonobese
individuals.
BMI Should Not Play a Central Role in
Eligibility for Bariatric Surgery
Current BMI cutoffs for bariatric surgery
stem from the National Institutes of
Health consensus statement, based
on a consensus development conference dating back to 1991 (45), where
the authors themselves state that
“there are insufficient data on which to
base recommendation for patient selection using objective clinical features
alone.” Despite significant improvements in surgical techniques and abundant data that have accumulated, the
same golden “BMI $40 or $35 kg/m2
with comorbidities” standard is still
practiced as originally recommended.
In the past few years, quite a few studies, nearly all performed in patients
with diabetes, have challenged the
“BMI $35 kg/m2” threshold for bariatric
surgery, while adopting the more appropriate designation “metabolic surgery.”
Many of these studies provide data
suggesting that the extraordinary beneficial impact these procedures have on
the control of diabetes, as well as on
other obesity-related metabolic conditions, still holds when the preoperative
BMI is ,35 kg/m2 (5,46–48).
The realization that patients with diabetes, who are not necessarily morbidly obese, may dramatically improve
glucose homeostasis via bariatric surgery raised the inevitable question of
whether BMI was the most appropriate
patient selection tool for metabolic surgery. It has been shown that BMI, determined by both fat and lean body
mass, does not necessarily predict metabolic status. Although there is much
overlap between obese individuals
care.diabetesjournals.org
(per BMI) and those having a high degree
of adiposity, a significant number of
obese individuals do not suffer from
metabolic syndrome (49,50) and are
now referred to as metabolically healthy
obese. On the other hand, less obese, or
nonobese, individuals may be found to
be more metabolically impaired. Individuals who share the same BMI do not
necessarily share the same degree of fatness and may have a very different fat
mass percentage as well as a different
fat distribution, with diverse metabolic
consequences. Visceral adiposity and
intramyocellular lipids as well as triglyceride content in the liver are more
strongly correlated to metabolic abnormalities, including insulin resistance,
compared with mere high BMI (51–54).
It is therefore not surprising that BMI,
being a relatively poor indicator of metabolic status, was not able to predict the
metabolic outcomes of bariatric surgery. The SOS cohort provided data
showing that patients undergoing bariatric surgery have a lower chance of
developing diabetes, cardiovascular
events, and cancer, as well as overall
mortality (34,35,55–58); however, in
neither of these studies has baseline
BMI been established as a predicting factor. This result underscores the limited
significance of presurgery BMI to the
outcomes of metabolic surgery. In another study based on the SOS cohort,
subjects were retrospectively divided
into groups deemed eligible or noneligible for bariatric surgery according to
current guidelines and were then assessed for the development of diabetes
and cardiovascular outcomes (57).
After a 10-year observation period, subjects qualifying for surgery under current
guidelines had a similar rate of diabetes
remission compared with those who did
not qualify (73 and 67%, respectively).
Briefly, this means that some patients
who would not be eligible for bariatric
surgery, according to the currently used
guidelines, could still have benefited
from the surgery. A meta-analysis looking
at 94 studies including 4,944 patients
with type 2 diabetes showed that bariatric
surgery led to similar rates of diabetes
remission in patients who had a baseline
BMI ,35 kg/m2 (72%) and in patients
who had a baseline BMI $35 kg/m 2
(71%) (59).
The IFSO recently released a position statement regarding bariatric
Segal-Lieberman, Segal, and Dicker
surgery in class 1 obesity, where the authors refer to BMI as “an inaccurate index of adiposity and a poor health risk
predictor” and state that in patients
with class 1 obesity associated with significant obesity-related comorbidities,
“access to bariatric surgery should not
be denied . . . simply on the basis of the
BMI level” (43), suggesting that the
“BMI-centric” attitude should be replaced by a more individualized, metabolically oriented approach in this
population.
Increased waist circumference is a
well-established predictor for development of type 2 diabetes (60–62), and
several studies have shown that it is a
superior predictor for diabetes development compared with BMI (63–65). In
the above-mentioned meta-analysis
(59), baseline waist circumference was
the only parameter that was correlated
with HbA 1c reduction after surgery;
counterintuitively, subjects starting
at a lower baseline waist circumference
benefited from a higher rate of HbA1c
reduction. The authors suggest that this
counterintuitive result may reflect a
study selection bias for patients with
higher HbA1c. It should be noted that
those patients with lower baseline
waist circumference, still undergoing
bariatric surgery, most likely had a
more advanced disease accompanied
by a higher HbA 1c. Nonetheless, this
study clearly shows that bariatric surgery is an equally effective diabetes
treatment in both the morbidly obese
and nonmorbidly obese population
with diabetes.
Taken together, these data suggest
that BMI is an outdated and probably
poor indicator for metabolic improvement after bariatric surgery and call for
finding more reliable indicators for selecting patients for bariatric surgery
based on metabolic status.
The Edmonton Obesity Staging System (EOSS) has been proposed as a
patient-selection tool more capable of
predicting the outcome of bariatric surgery compared with anthropometric
measures such as BMI or waist circumference. This system takes into account
the severity of the obesity-related
comorbidities, as well as the functional
and mental status of the obese patient
considering bariatric surgery (66). According to this system, the patient is
assigned a stage from 0 to 4, wherein
stage 0 describes a patient with no apparent obesity-related comorbidities, no
physical symptoms or psychopathology,
and no functional limitations or impaired
well-being related to obesity and stage 4
describes a patient with severe disabilities due to obesity-related comorbidities, severe psychopathology, physical
limitations, and/or severe impairment
of well-being. Using the criteria of the
EOSS, Kuk et al. (67) found that obese
subjects assigned to stage 0–1 did not
show an increase in mortality risk,
whereas subjects assigned to stage 2
or 3 had an increased all-cause as well
as cardiovascular-related mortality
risk.
Another study assessed the capacity
of the EOSS to predict mortality analyzed data from the National Health
and Nutrition Examination Surveys
(NHANES) (68). In this cohort, patients
assigned to stages 2 and 3 had an increased mortality risk (with a hazard
ratio of 1.57 and 2.69, respectively)
compared with patients assigned to
stages 0 and 1, even after adjustment
for BMI and the metabolic syndrome;
this was true also in a cohort eligible
for bariatric surgery. These studies
show that patients sharing the same
BMI may exhibit diverse cardiometabolic risks and may suggest that care
providers, in selecting their treatment
regimens, should prioritize patients
at risk over merely obese individuals. Interestingly, in a study applying
the criteria of the EOSS to a cohort of
5,787 patients attending a weightmanagement clinic, it was found that
the stage approach could predict one’s
ability to lose weight (69). Patients
assigned to stage 0–1 lost weight more
easily and rapidly than those assigned
to stages 2 and 3, thereby providing a
weight-independent tool for the prediction of weight loss. This observation led
to the notion that the EOSS may replace
BMI as a better tool for selecting patients who can benefit from bariatric
surgery (70).
Lastly, like other surgeries, bariatric
surgery also entails complications, and
that risk should be taken into account on
an individual basis while selecting the
most suitable candidates for surgery.
The King’s College criteria offer a holistic
method for assisting perioperative complications by gathering all physical, mental, social, and financial information (71);
S271
S272
BMI as a Criteria for Bariatric Surgery
however, this approach may suffer from
practical limitations stemming from inherent difficulties in data collection.
The ultimate bariatric eligibility scale,
enabling an optimal selection of candidates for bariatric surgery, based on
validated hard outcomes, such as cardiovascular disease, complication rate,
and mortality, is yet to be established.
However, a compilation of a robust
bariatric eligibility scale that will be incorporated into the metabolic surgery preoperative assessment and replace the
BMI criteria seems to gather momentum.
Conclusions
It is the authors’ opinion, based on current available information, that the following criteria should be used for
selecting patients for bariatric surgery:
1) BMI .40 kg/m2, 2) BMI .35 kg/m2
plus comorbidities, 3) BMI 30–35 kg/m2
and uncontrolled diabetes, 4) BMI 30–
35 kg/m2 plus EOSS stage .2 subject to
the practitioner’s clinical judgment, and
5) exclusion of BMI ,30 kg/m2 subject
to further research.
It is important to emphasize that at
present there are no guidelines recommending bariatric surgery in nonobese
patients, and this procedure is considered investigational and preliminary in
this population.
We hope for elucidation of the mechanisms acting in bringing about the
remission of diabetes after bariatric surgery, which will hopefully enable further
refinement of the selection process of
candidates for bariatric surgery.
Duality of Interest. No potential conflicts of
interest relevant to this article were reported.
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