Cell Biochem Biophys (2007) 48:97102

DOI 10.1007/s12013-007-0020-y

ORIGINAL PAPER

Impact of bariatric surgery on type 2 diabetes

Luigi Fernando Meneghini

Published online: 17 April 2007

Humana Press Inc. 2007

Abstract The management and prevention of diabetes

through lifestyle modifications and weight loss should be
the mainstay of therapy in appropriate candidates.
Although the results from the Diabetes Prevention Trial
and the Finnish Prevention Study support this approach,
over 95% of patients not participating in a prevention
research study are unable to achieve and maintain any
significant weight loss over time. Bariatric surgery for
weight loss is an emerging option for more sustainable
weight loss in the severely obese subject, especially when
obesity is complicated by diabetes or other co-morbidities.
The two most common types of procedures currently used
in the United States are adjustable gastric bands and
Roux-en-Y gastric bypass. These procedures can be performed laparoscopically, further reducing the perioperative
morbidity and mortality associated with the surgery. While
the gastric bypass procedure usually results is greater
sustained weight loss (4050%) than adjustable gastric
banding (2030%), it also carries greater morbidity and
nutritional/metabolic issues, such as deficiencies in iron,
B12, calcium, and vitamin D. Following bariatric surgery
most subjects experience improvements in diabetes control,
hypertension, dyslipidemia, and other obesity-related
conditions. In patients with impaired glucose tolerance
most studies report 99100% prevention of progression to
diabetes, while in subjects with diabetes prior to surgery,
resolution of the disease is reported in 6493% of the cases.
While improvements in insulin resistance and beta-cell
function are related to surgically induced weight loss, the
rapid post-operative improvement in glycemia is possibly
L. F. Meneghini (&)
Diabetes Research Institute, University of Miami
Miller School of Medicine, Miami, FL, USA
e-mail: lmeneghi@med.miami.edu

due to a combination of decreased nutrient intake and

changes in gut hormones as a result of the bypassed
intestine. Post-prandial hyperinsulinemic hypoglycemia
associated with nesidioblastosis has been described in a
series of patients following gastric bypass surgery, and may
be related to the described changes in GLP-1 and other gut
hormones.
Keywords Weight loss
Bariatric surgery
Gastric
bypass
Gastric banding
Diabetes
Impaired glucose
tolerance
Glucagon-like Peptide 1 (GLP-1)

Obesity is a major risk factor and health challenge for the

developed and developing world. As the average weight of
the population increases, so does the prevalence of
hypertension, cardiovascular disease, and diabetes, among
other things. In the United States, over 30% of the population is considered obese (BMI 30 kg/m2), with almost
5% of them having a BMI of 40 kg/m2 or more (severely
obese) [1]. Not surprisingly, in individuals with diabetes,
these statistics are even more alarming with one survey
revealing half of a population with diabetes meeting the
obese criteria and 9% falling into the severely obese
category [2].
Weight loss in the overweight or obese patient can delay
or even prevent the onset of diabetes in individuals with
pre-diabetes or impaired glucose tolerance (IGT), and
significantly improve glycemic levels in subjects with type
2 diabetes [35]. Aggressive treatment of type 2 diabetes
has clearly been shown to reduce morbidity and mortality
and improve long-term quality of life, [67] nevertheless
the management of hyperglycemia, obesity, and related
abnormalities can be a challenging experience for both
patient and physician. Of note is that the American

98

Diabetes Association (ADA) mandated goal of HbA1c

<7% is achieved by less than half of patients with diabetes
[8], and despite an improved anti-glycemic arsenal of oral
agents and insulin, diabetes control continues to be dismal
[9].
Prevention and treatment of obesity and diabetes
through effective public health lifestyle initiatives should
be of imminent priority. Unfortunately, the clinical interventions currently available to address obesity, through
nutrition and lifestyle changes combined, when appropriate, with anti-obesity agents and behavior modifications,
produce only modest weight loss (510% loss of excess
body weight), which is seldom sustainable over the long
run [1012]. This is especially true in individuals with
diabetes [13]. In addition, patient expectations of what is
considered desirable or acceptable weight loss (2532%
actual loss of body weight) far exceeds the outcomes
achieved using traditional therapies [14]. The difficulty
with weight loss through medical intervention and the
realization of the limited outcomes of these efforts, has led
to consideration of more invasive interventions. Of note
that weight loss in the literature is at times reported as %
[actual] weight loss or % excess weight loss. For example,
a 200 pound individual whose ideal body weight is
150 pounds has an excess body weight of 50 pounds. If
that individual loses 25 pounds, this can be either reported
as a 12.5% loss of weight or a 50% loss of excess body
weight.
Reports in the literature on outcomes of bariatric surgery
for the treatment of obesity demonstrate accumulating data
which indicates not only considerable and sustained weight
loss following this type of intervention, but also the associated resolution of obesity-related complications, such as
type 2 diabetes, hypertension and dyslipidemia. In the
following article we will discuss the most common
bariatric procedures done in the US and review the
outcomes and complications of these interventions in
subjects with type 2 diabetes.
The number of bariatric procedures performed in this
country has steadily risen from about 16,000 in the early
1990s to approximately 103,000 in 2003 [15], with as
many as 130,000 expected by 2005 [16]. Although gastric
bypass accounted for more than 80% of all bariatric
procedures in the US [16], adjustable gastric banding
(Lap-Band), which was approved by the FDA in 2001 is
gaining popularity, and has been widely used abroad for the
past decade [17]. The recipients of bariatric procedures in
this country appear to be predominantly female (~80%),
subjects with private insurance and with the highest
household incomes [16].
The principles for weight loss through surgery rely on
gastric volume restriction, intestinal malabsorption, or a
combination of both. The two most common weight loss

Cell Biochem Biophys (2007) 48:97102

surgeries currently performed in the United States are

gastric bypass and gastric banding. Adjustable gastric
banding, which is a purely restrictive procedure, uses a
band-like, saline-filled tube that encircles the upper part of
the stomach, creating a small pouch of 1520 cc that limits
that amount of food that can be comfortably ingested by a
patient. The Lap-Band is placed laparoscopically and can
be adjusted subsequently based on patient response and
adverse events (weight loss, vomiting, esophageal
enlargement). Being less invasive, AGB has the lowest
mortality rate (00.7%) and is expected to result in an
average excess weight loss of 3060%.
Gastric bypass, on the other hand, is a combination of a
restrictive procedure with some degree of malabsorption.
The FDA recommended Roux-en-Y gastric bypass
(RYGBP) is achieved by creating a small gastric pouch that
is separated by staples from the rest of the stomach and
anastomosing the small pouch to the distal portion of the
jejunum, thereby decreasing nutrient absorption. The
length of bypassed intestine can be adjusted according to
the desired amount of malabsorption and subsequent
weight loss. Although RYGBP is increasingly done
through a laparoscopic approach, gastric bypass still
occasionally requires an open incision technique. RYGBP
carries a slightly higher mortality rate (03.3%) than AGB,
but usually results in greater average excess weight loss
(5080%), which has been shown to be sustained over time
[17]. Contributors to the higher morbidity and mortality of
RYGBP appear to include advanced patient age, male
gender and lower surgeon (or hospital) volume of bariatric
procedures [18].
With regards to health care utilization following bariatric procedures, the data are mixed. A recent survey of
subjects undergoing RYGBP reported a significant increase
in hospitalizations in the year following surgery compared
to pre-surgery (19% vs. 8%), mostly for complications
thought to be related to the surgery (ventral hernia repair,
gastric revision] [19]. On the other hand, a study done by
Christou and colleagues reported reduced rates of hospitalization over 5 years following RYGBP surgery, with
concomitant reductions in health care costs when compared
to matched controls [20]. In the Swedish Obese Subjects
(SOS) Intervention, a predominantly gastric banding
intervention, a comparison of the pharmaceutical utilization between subjects having undergone bariatric surgery
and a control group showed similar costs [21]. The
decrease in use of drugs to treat diabetes and cardiovascular conditions were offset by an increase use in
medications to manage gastrointestinal tract disorders.
Complications following bariatric surgery are often
related to surgical issues in the year following the surgery,
and to nutritional and metabolic issues in the longer
term [22]. The most common complications following

Cell Biochem Biophys (2007) 48:97102

Lap-Band procedures include esophageal dilatation (up to

71%), gastric prolapse (up to 24%), gastric outlet
obstruction (up to 14%), and gastric band revision (up to
14%) [17]. With laparoscopic RYGBP the problems are
related to anastomotic strictures and bowel obstruction (up
to 11%), wound infection (up to 9%) and conversion to an
open procedure (up to 8%). Symptoms common during the
first year following weight loss surgery include vomiting,
dumping syndrome, dehydration, occasional protein malnutrition, hair loss, and gallstone formation. Longer term
issues, mostly related to the mild malabsorption following
RYGBP include deficiencies in vitamin B12 and iron
(anemia and peripheral neuropathy), vitamin D (secondary
hyperparathyroidism and osteomalacia) as well as folate
and thiamine. Dumping syndrome, characterized by
symptoms such as post-prandial fatigue, weakness, sweating, tachycardia, and dizziness can occur within 30 min of
the meal (early dumping) or later (late dumping). In many
cases symptoms of late dumping may actually reflect an
episode of reactive hypoglycemia [23]. A few recent reports have ascribed post-prandial hypoglycemia following
gastric bypass surgery to the finding of nesidioblastosis on
pathology reports of partially pancreatectomized subjects
[2425]. An interesting association, which has been documented in a few studies, is the supraphysiologic rise in
post-prandial GLP-1 levels seen in subjects following
gastrectomy [2627]. Given its potent anti-glycemic effects
through glucose-dependent insulin secretion of beta cells,
and the observation of islet neogenesis and decreased
apoptosis in animal and in vitro human studies, GLP-1 may
have a role in exacerbating this syndrome [2829].
Bariatric surgery is indicated for the treatment of obesity
in subjects who have documented failure of a non-surgical
approach to weight loss and whose BMI is 40 kg/m2,
or 35 kg/m2 with associated co-morbid conditions such
as diabetes, hypertension, dyslipidemia, cardiovascular
disease, obstructive sleep apnea, urinary incontinence, and
osteoarthritis. In addition, patients should have clear
expectations of the benefits and complications of surgery,
should be psychologically stable and should be willing to
engage in healthy lifestyle and nutrition habits following
the surgery. A supportive family and social environment is
also of benefit. The NIH consensus panel which defined the
selection criteria for bariatric surgery in 1991 [12] was
reconvened in 2004 to update these guidelines (report not
available as of date of this article publication).
Although there are some differences in the metabolic
response following AGB and RYGBP, the impact of either
procedure on diabetes and IGT is significant. In both
interventions, the weight loss that follows surgery appears
to improve both insulin resistance and beta-cell function,
with consequent improvement in glycemic control as
manifested by resolution of diabetes in many cases and

99

non-progression from IGT to diabetes in most instances. In

a 1 year study by Dixon and colleagues [32] using
adjustable laparoscopic banding, improvement in insulin
sensitivity closely correlated with weight loss, while
improvement in beta-cell function were more closely
associated with duration of diabetes. In this and other
studies, the greatest benefit with regard to glycemic control
is often obtained early in the disease process, when weight
loss is achieved before beta-cell function is permanently
impaired [3033] . In another report, Polyzogopoulou [33]
and colleagues demonstrated a restoration of first phase
insulin release (935% increase in acute insulin response
compared to baseline) and normalization of insulin sensitivity in subjects with mild to moderate diabetes associated
with a 46% reduction in body weight 12 months following
gastric bypass surgery. The relationship between insulin
sensitivity and acute insulin response was also normalized
and similar to that of matched non-diabetic controls, and all
subjects with either impaired glucose tolerance or diabetes
experienced normalization of their fasting plasma glucose.
While in AGB the improvement in metabolic status
appears to be directly related to subsequent weight loss, in
RYGBP substantial improvements in metabolic parameters
actually occur soon after surgery and before any significant
weight loss has occurred [34]. Considerable interest and
research is now focusing on identifying the reasons for this
early reversal of metabolic abnormalities, including defining the role of hormones that affect satiety, beta-cell
function, and insulin resistance, such as ghrelin, leptin,
adiponectin, resistin, Glucagon-like Peptide 1 (GLP-1), and
Gastric Inhibitory Polypeptide (GIP) [3537] .
The largest and most complete study evaluating the
short- and long-term effects of bariatric surgery is the
Swedish Obese Subjects (SOS) intervention, which
published 10-year data on 641 subjects who predominantly
underwent a gastric restrictive procedure (gastric banding
24% or vertical banded gastroplasty 70%) [38]. The surgical subjects on average lost 23.4% of their total body
weight by 2 years and maintained 16.5% weight loss at
10 years, compared to an increase of 0.1% and 1.6%,
respectively in the control group. At 10 years, compared to
the control group, the surgical group had a statistically
significant odds ratio for recovery from diabetes (3.45),
hypertension (1.68), hypertriglyceridemia (2.57), and low
HDL cholesterol (2.35). Recovery from hypercholesterolemia (OR 1.30) did not reach statistically significance. The
5% of subjects in the surgery group who underwent gastric
bypass had an even more impressive weight loss of 25% at
10 years. This translated into clinically and statistically
significant reductions, compared to gastric banding, in triglycerides (18.0% vs. 28.0%), HDL cholesterol (20.4%
vs. 47.5%), and total cholesterol (5.0% vs. 12.6%)
levels. Although the primary outcome of the study was a

100

difference in mortality between the surgery subjects and

the matched controls, at the time of publication of the data
the authors claimed that not enough subjects had completed
the study to show a statistical difference.
A number of reports on gastric bypass surgery have been
published in the literature, and although the data are not
presented in a standardized fashion, the outcomes with
respect to diabetes resolution or prevention are remarkable
[39]. Long and colleagues [31] followed 136 obese subjects
with IGT for an average of 6 years (109 underwent open
gastric bypass while 27 served as voluntary controls) and
showed that while 22% of the control group developed
diabetes, only 1 (0.9%) patient from the surgical cohort
did. This was achieved through a 52% loss of excess
weight over that period of time. Pories and et al. [30]
followed 608 severely obese subjects for an average of
8 years following open gastric bypass and reported that of
the 165 subjects with diabetes 83% had a normal A1C by
study end (no mention of anti-diabetic medications is
made), and of the 165 with IGT, 99% reverted to euglycemia. The average excess weight loss at 14 years in this
study was 49%. Other studies examining the effects of
gastric bypass on abnormal glucose tolerance report anywhere from a 7193% resolution of diabetes associated
with a 3338% decrease in body weight [4042].
In a recent review and meta-analysis of bariatric
surgery, Buchwald and colleagues [43] summarized the
outcomes related to each specific procedure. Resolution of
diabetes was defined across studies as the ability to discontinue diabetes-related medications and maintain blood
glucose levels within the normal range. From this analysis, it becomes apparent that in subjects with diabetes or
impaired glucose tolerance, gastric bypass was consistently
more effective at improving or reversing hyperglycemia.
For example, almost twice as many subjects experience
resolution of diabetes with gastric bypass than with gastric
banding (83.7% vs. 47.9%, respectively). This observation
is not completely explained by the greater excess weight
loss seen with gastric bypass, but may in fact relate to
differential effects on gut hormones resulting from
bypassing the foregut.
It is clear that weight loss, especially when combined
with physical activity, is effective at both delaying the
progression from IGT to diabetes and in controlling
glycemia in subjects with type 2 diabetes. The current
evidence demonstrates a substantially better outcome with
regards to weight loss, and consequently metabolic control,
with weight loss surgery than with available non-surgical
approaches. For example, the 6% weight loss achieved in
the lifestyle intervention cohort of the DPP is dwarfed by
the 2038% average weight loss observed in bariatric
procedures performed today in the USA [39]. Likewise, the
58% reduction in progression to diabetes in the DPP

Cell Biochem Biophys (2007) 48:97102

appears minimal compared to the almost 100% non-progression reported in the bariatric literature. Also of note is
that outcomes from lifestyle intervention were made
possible within an experimental, subsidized environment
unlikely to be reproducible in the broader clinical arena.
In any case, regardless of the intervention, these studies
and supporting data propose that any intervention, whether
surgical or non-surgical, for the treatment of obesity-related type 2 diabetes has the most beneficial effect early
in the disease process before beta-cell function is
substantially impaired and before the onset of chronic
complications. The evidence suggests that both gastric
banding and gastric bypass interventions have a positive
impact on the prevention and progression of type 2 diabetes
and obesity-related co-morbid conditions. The effects of
bariatric surgery on long-term patient mortality remains yet
to be more clearly defined.
In conclusion, bariatric surgery appears to be an effective and beneficial intervention in selected obese
(BMI > 35 kg/m2) patients with diabetes, when medical
and nutritional approaches have failed to achieve the
desired outcomes. This becomes especially true when
metabolic control in these individuals has not been
achieved despite aggressive medical therapy. In addition,
in obese individuals with pre-diabetes, weight loss through
the bariatric approach is clearly an extremely effective
intervention to prevent progression to diabetes.

References
1. Hedley, A. A., Ogden, C. I., Johnson, C. L., Carroll, M. D.,
Curtin, L. R., & Flegal, K. M. (2004). Prevalence of overweight
and obesity among us children, adolescents, and adults, 1999
2002. JAMA, 291, 28472850.
2. Leibson, C. L., Williamson, D. F., Melton, L. J., Palumbo, P. J.,
Smith, S. A., Ramson, J. E., Schilling, P. L., & Narayan, K. M.
(2001). Temporal trends in BMI among adults with diabetes.
Diabetes Care, 24, 15841589.
3. Tuomilehto, J., Lindstrom, J., Eriksson, J. G., Valle, T. T.,
Hamalainen, H., Ilanne-Parikka, P., Keinanen-Kiukaaniemi, S.,
Laakso, M., Louheranta, A., Rastas, M., Salminen, V., & Uusitura, M. for the Finnish Diabetes Prevention Study Group (2001).
Prevention of type 2 diabetes mellitus by changes in lifestyle
among subjects with impaired glucose tolerance. N. Engl. J.
Med., 344, 13431350.
4. Eriksson, J., Lindstrom, J., & Tuomilehto, J (2001). Potential for
the prevention of type 2 diabetes. British Medical Bulletin, 60,
183199.
5. Diabetes Prevention Program Research Group (2002). Reduction
in the incidence of type 2 diabetes with lifestyle intervention or
metformin. The New England Journal of Medicine, 346, 393
403.
6. UK Prospective Diabetes Study Group (1998). Intensive bloodglucose control with sulphonylureas or insulin compared with
conventional treatment and risk of complications in patients with
type 2 diabetes. Lancet, 352, 837853.

Cell Biochem Biophys (2007) 48:97102

7. The Diabetes Prevention Program Research Group (2005). Impact of intensive lifestyle and metformin therapy on cardiovascular disease risk factors in the Diabetes Prevention Program.
Diabetes Care, 28, 888894.
8. Saaddine, J. B., Engelgau, M. M., Beckles, G. L., Gregg, E. W.,
Thompson, T. J., & Venkat Narayan, K. M. (2002). A diabetes
report card for the United States: Quality of care in the 1990s.
Annals of Internal Medicine, 136, 565574.
9. Koro, C. E., Bowlin, S. J., Bourgeois, N., & Fedder, D. O. (2004).
Glycemic control from 1988 to 2000 among U.S. adults diagnosed with type 2 diabetes Diabetes Care, 27, 1720.
10. Leibbrand, R., & Fichter, M. M. (2002). Maintenance of weight
loss after obesity treatment: is continuous support necessary?
Behaviour Research and Therapy, 40, 12751289.
11. Zimmet, P., Shaw, J., & Alberti, K. G. (2003). Preventing type 2
diabetes and the dysmetabolic syndrome in the real world: a
realistic view. Diabetic Medicine, 20, 693702.
12. NIH Conference (1991). Gastrointestinal surgery for severe
obesity. Consensus development conference panel. Annals of
Internal Medicine, 115, 956961.
13. Wing, R. R., Marcus, M. D., Epstein, L. H., & Salata, R. (1987).
Type II diabetic subjects lose less weight than their overweight
nondiabetic spouses. Diabetes Care, 10, 563566.
14. Foster, G. D., Wadden, T. A., Vogt, R. A., & Brewer, G. (1997).
What is a reasonable weight loss? Patients expectations and
evaluations of obesity treatment outcomes. Journals of Consulting and Clinical Psychology, 65, 7985.
15. Steinbrook, R. (2004). Surgery for severe obesity. The New
England Journal of Medicine, 350, 10751079.
16. Santry, H. P., Gillen, D. L., & Lauderdale, D. S. (2005). Trends in
bariatric surgical procedures. JAMA, 294, 19091917.
17. Schneider, B. E., & Mun, E. C. (2005). Surgical management of
morbid obesity. Diabetes Care, 28, 475480.
18. Flum, D. R., Salem, L., Broeckel Elrod, J. A., Dellinger, E. P.,
Cheadle, A., & Chan, L. (2005). Early mortality among Medicare
beneficiaries undergoing bariatric surgical procedures. JAMA,
294, 19031908.
19. Zingmond, D. S., McGory, M. L., & Ko, C. Y. (2005).
Hospitalization before and after bypass surgery. JAMA, 294,
19181924.
20. Christou, N. V., Sampalis, J. S., Liberman, M., Look, D., Auger,
S., McLean, A. P. H., & MacLean, L. D. (2004). Surgery
decreases long-term mortality, morbidity and health care use in
morbidly obese patients. Annals of Surgery, 240, 416424.
21. Narbro, K., Agren, G., Jonsson, E., Naslund, I., Sjostrom, L., &
Peltonen, M. (2002). Pharmaceutical costs in obese individuals:
Comparison with a randomly selected population sample and
long-term changes after conventional and surgical treatmentthe
SOS intervention study. Archives of Internal Medicine, 162,
20612069.
22. Fujioka, K. (2005). Follow-up of nutritional and metabolic
problems after bariatric surgery. Diabetes Care, 28, 481484.
23. Wapnick, S., & Joness, J. J. (1972). Changes in glucose tolerance
and serum insulin following partial gastrectomy and intestinal
resection. Gut, 13, 871873.
24. Service, G. F., Thompson, G. B., Service, F. J., Andrews, J. C.,
Collazo-Clavell, M. L., & Lloyd, R. V. (2005). Hyperinsulinemic
hypoglycemia with nesidioblastosis after gastric-bypass surgery.
The New England Journal of Medicine, 353, 249254.
25. Patti, M. E., McMahon, G., Mun, E. C., Bitton, A., Holst, J. J.,
Goldsmith, J., Hanto, D. W., Callery, M., Arky, R., Nose, V.,
Bonner-Weir, S., & Goldfine, A. B. (2005). Severe hypoglycemia
post-gastric bypass requiring partial pancreatectomy: Evidence
for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia, 48, 22362240.

101
26. Miholic, J., Orskov, C., Holst, J. J., Kotzerke, J., & Meyer, H. J.
(1991). Emptying of the gastric substitute, Glucagon-like Peptide-1 (GLP-1), and reactive hypoglycemia after total gastrectomy. Digestive Diseases and Sciences, 36, 13611370.
27. Gebhard, B., Holst, J. J., Biegelmayer, C., & Miholic, J. (2001).
Postprandial GLP-1, norepinephrine, and reactive hypoglycemia
in dumping syndrome. Digestive Diseases and Sciences, 46,
19151923.
28. Farilla, L., Bulotta, A., Hirshberg, B., Li Calzi, S., Khoury, N.,
Noushmehr, H., Bertolotto, C., Di Mario, U., Harlan, D. M., &
Perfetti, R. (2003). Glucagon-like Peptide 1 inhibits cell apoptosis and improves glucose responsiveness of freshly isolated
human islets. Endocrinology, 144, 51495158.
29. Brubaker, P. L., & Drucker, D. J. (2004). Minireview: Glucagonlike polypeptides regulate cell proliferation and apoptosis in the
pancreas, gut and central nervous system. Endocrinology, 145,
26532659.
30. Pories, W. J., Swanson, M. S., MacDonald, K. G., Long, S. B.,
Morris, P. G., Brown, B. M., Barakat, H. A., deRamon, R. A.,
Israel, G., & Dolezal, J. M. (1995). Who would have thought it?
An operation proves to be the most effective therapy for adult
onset diabetes mellitus. Annals of Surgery, 222, 339352.
31. Long, S., OBrien, K., MacDonald, K. G. Jr, Leggett-Frazier, N.,
Swanson, M. S., Pories, W. J., & Caro, J. F. (1994). Weight loss
in severely obese subjects prevents progression of impaired glucose tolerance to type II diabetes. Diabetes Care, 17, 372375.
32. Dixon, J. B., & OBrien, P. E. (2002). Health outcomes of severely obese type 2 diabetic subjects 1 year after laparoscopic
adjustable gastric banding. Diabetes Care, 25, 358363.
33. Polyzogopoulou, E. V., Kalfarentzos, F., Vagenakis, A. G., &
Alexandrides, T. K. (2003). Restoration of euglycemia and normal acute insulin response to glucose in obese subjects with type
2 diabetes following bariatric surgery. Diabetes, 52, 10981103.
34. Hickey, M. S., Pories, W. J., MacDonald, K. G., Cory, K. A.,
Dohm, G. L., Swanson, M. S., Israel, R. G., Barakat, H. A.,
Considine, R. V., Caro, J. F., & Houmard, J. A. (1998). A new
paradigm for type 2 diabetes mellitus: could it be a disease of the
foregut? Annals of Surgery, 227, 637644.
35. Kellum, J. M., Kuemmerle, J. F., ODorisio, T. M., Rayford,
P., Martin, D., Engle, K., Wolf, L., & Sugerman, H. J. (1990).
GI hormone response to meals before and after gastric bypass
and vertical banded gastroplasty. Annals of Surgery, 211, 763
771.
36. Rubino, F., & Gagner, M. (2002). Potential of surgery for curing
type 2 diabetes mellitus. Annals of Surgery, 236, 554559.
37. Faraj, M., Havel, P. J., Phelis, S., Blank, D., Sniderman, A. D., &
Cianflone, K. (2003). Plasma acylation-stimulating protein,
adiponectin, leptin, and ghrelin before and after weight loss induced by gastric bypass surgery in morbidly obese subjects. The
Journal of Clinical Endocrinology and Metabolism, 88, 1594
1602.
38. Sjostrom, L., Lindroos, A. K., Peltonen, M., Torgerson, J.,
Bouchard, C., Carlsson, B., Dahlgreen, S., Larsson, B., Narbro,
K., Sjostrom, C. D., Sullivan, M., & Wedel, H. for the SOS Study
Scientific Group (2004). Lifestyle, diabetes and cardiovascular
risk factors 10 years after bariatric surgery. The New England
Journal of Medicine, 351, 26832693.
39. Ferchak, C. V., & Meneghini, L. F. (2004). Obesity, bariatric
surgery and type 2 diabetes: a systematic review. Diabetes
Metabolism Research and Reviews, 20, 438445.
40. Cowan, G. S., & Buffington, C. K. (1998). Significant changes in
blood pressure, glucose and lipids with gastric bypass surgery.
World Journal of Surgery, 22, 987992.
41. DeMaria, E. J., Sugarman, H. J., Kellum, J. M., Meador, J. G., &
Wolfe, L. G. (2002). Results of 281 consecutive total laparo-

102
scopic Roux-en-Y gastric bypasses to treat morbid obesity.
Annals of Surgery, 235, 640647.
42. MacDonald, K. G. Jr., Long, S. D., Swanson, M. S., Brown, B.
M., Morris, P., Dohm, G. L., & Pories, W. J. (1997). The gastric
bypass operation reduces the progression and mortality of

Cell Biochem Biophys (2007) 48:97102

non-insulin dependent diabetes mellitus. Gastrointestinal Surgery, 1, 213220.
43. Buchwald, H., Avidor, Y., Braunwald, E., Jensen, M. D., Pories,
W., Fahrbach, K., & Schoelles, K., (2004). Bariatric surgery: A
systematic review and meta-analysis. JAMA, 292, 17241737.