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Original Article |
Università degli Studi di Milano (A.E.P., P.P., M.G.), Cattedra di Medicina Interna; Second Divisione di Medicina Interna (A.E.P., P.P.), Ospedale San Paolo, 20142, Milano; Divisione di Medicina Interna (M.C.L., P.V., M.M., F.F.) and Servizio di Radiologia (E.C., C.O.), Istituto di Ricovero e Cura a Carattere Scientifico Ospedale San Raffaele; and Ateneo Vita-Salute (M.P., G.F.), Cattedra di Chirurgia Generale, 20132 Milano, Italy
Address all correspondence and requests for reprints to: A. E. Pontiroli, M.D., Medicina 2°, Ospedale San Paolo, Via A Di Rudinì 8, 20142 Milano, Italy. E-mail: . antonio.pontiroli{at}unimi.it
Abstract
Weight loss ameliorates arterial hypertension and glucose metabolism in obese patients, but the dietary approach is unsatisfactory because obesity relapses. Durable reduction of body weight, obtained through major nonreversible surgical procedures, such as jejunal and gastric bypass, allows improvement of glucose metabolism and arterial blood pressure in morbid (grade 3) obesity. Laparoscopic adjustable gastric banding (LAGB) is a minimally invasive and reversible surgical procedure that yields a significant reduction of gastric volume and hunger sensation. In this study, 143 patients with grade 3 obesity [27 men and 116 women; age, 42.9 ± 0.83 yr; body mass index (BMI), 44.9 ± 0.53 kg/m2; normal glucose tolerance (NGT; n = 77); impaired glucose tolerance (IGT; n = 47); type 2 diabetes mellitus (T2DM; n = 19)] underwent LAGB and a 3-yr follow-up for clinical (BMI, waist circumference, waist to hip ratio, and arterial blood pressure) and metabolic variables (glycosylated hemoglobin, fasting insulin and glucose, insulin and glucose response to oral glucose tolerance test, homeostasis model assessment index, total and high-density lipoprotein cholesterol, triglycerides, uric acid, and transaminases). At baseline and 1 yr after LAGB, patients underwent computerized tomography and ultrasound evaluation of visceral and sc adipose tissue. One-year metabolic results were compared with 120 obese patients (51 men and 69 women; age, 42.9 ± 1.11 yr; BMI, 43.6 ± 0.46 kg/m2; NGT, n = 66; IGT, n = 8; T2DM, n = 46) receiving standard dietary treatment. LAGB induced a significant and persistent weight loss and decrease of blood pressure. Greater metabolic effects were observed in T2DM patients than in NGT and IGT patients, so that at 3 yr glycosylated hemoglobin was no longer different in NGT and T2DM subjects. Clinical and metabolic improvements were proportional to the amount of weight loss. LAGB induced a greater reduction of visceral fat than sc fat. At 1-yr evaluation, weight loss and metabolic improvements were greater in LAGB-treated than diet-treated patients. We conclude that LAGB is an effective treatment of grade 3 obesity in inducing long-lasting reduction of body weight and arterial blood pressure, modifying body fat distribution, and improving glucose and lipid metabolism, especially in T2DM.
OVERWEIGHT IS A MAJOR problem in Western countries. In the United States, 32.6% of adults meet the World Health Organization definition of grade 1 overweight [a body mass index (BMI) between 25.0 and 29.9 kg/m2], and 22.3% meet the criteria for grade 2 and grade 3 overweight (BMI 
30.0; Ref. 1). In addition, between National Health and Nutrition Examination Survey (NHANES) II and NHANES III, the prevalence of obesity (BMI >30.0 kg/m2) rose from 14.5% to 22.5% (1, 2). The use of standardized definitions facilitates international comparisons, and these findings are in agreement with trends seen elsewhere in the world, where obesity affects up to 18% of people in Western countries, and its incidence is increasing (3).
Obese subjects are at increased risk of premature death from almost all causes (cancer, cardiovascular diseases, and other causes; Refs. 4 , 5). In addition, comorbidities affect up to 70% of obese people, and this worsens their overall prognosis (NHANES III, data unpublished). The frequency of comorbidities also raises the question whether the duration of obesity is a critical factor in their development; in particular, there is evidence linking duration of obesity to the development of type 2 diabetes mellitus (T2DM; Refs. 6, 7, 8, 9, 10) and to complications of arterial hypertension such as left ventricular hypertrophy (11, 12).
An unchallenged concept is that treatment of obesity based on dietary measures is unsatisfactory because obesity relapses. In particular, treatment of diabetes in obese patients is disappointing; at some point of the natural history of the disease, currently available oral hypoglycemic agents and dietary measures are insufficient in controlling hyperglycemia (13). However, insulin treatment in these patients promotes weight gain, increases arterial blood pressure, and worsens insulin resistance (13, 14), promoting a vicious circle in which increasing insulin doses do not achieve adequate control of glucose metabolism (15, 16). On the contrary, stable reduction of body weight can control T2DM and arterial hypertension (13, 17); these effects are likely to be mediated by a decrease of insulin resistance (13).
Bariatric surgery is a way to achieve stable reduction of body weight in morbidly (grade 3) obese patients. Surgical approaches can be divided into two categories: measures to reduce food absorption (jejunal bypass, biliary diversion) and to reduce food ingestion (gastric bypass). The latter has proven effective in preventing progression from impaired glucose tolerance (IGT) to T2DM (18), and in the long-term control of T2DM and of arterial hypertension (17). One should, however, realize that these effects were reached only through major nonreversible surgical procedures that bear significant morbidity and decrease the quality of life (17, 19).
Laparoscopic adjustable gastric banding (LAGB) is a minimally invasive surgical procedure; it consists of the placement of a silicone band around the gastric body. The result is a drastic reduction of the volume of the body of the stomach, which increases satiety sensation. The procedure is performed under general anesthesia and is completely reversible. The silicone band can be left in situ for up to 10 yr. LAGB is now regularly applied in a few European centers, and it has been recently approved by the Food and Drug Administration in the United States. Preliminary reports suggest that LAGB induces weight loss in a significant number of patients (20, 21, 22).
The aim of the present study was to evaluate long-term clinical and metabolic benefits of LAGB in patients with grade 3 obesity, especially in the presence of IGT and T2DM.
Patients and Methods
LAGB-treated patients
Since June of 1996, LAGB is regularly performed at the Istituto San Raffaele, Milano, Italy, in patients with morbid obesity, i.e. grade 3 obesity according to World Health Organization criteria (22, 23). According to the protocol approved by the local ethics committee, patients are eligible for LAGB when fulfilling the following criteria: age, 18–66 yr inclusive; BMI, greater than 40.0 kg/m2, or greater than 35.0 kg/m2 in the presence of comorbidities (24); and history of at least two previous attempts to lose weight with dietary and medical measures followed by relapse of obesity. Exclusion criteria are: obesity secondary to endocrinopathies (Cushing’s disease or syndrome, hypothyroidism), gastrointestinal inflammatory diseases, risk of upper gastrointestinal bleeding, pregnancy, alcohol or drug addiction, and previous or current malignancies. Two oral glucose tolerance tests (OGTTs; 75 g) are performed in all patients for whom a diagnosis of IGT or T2DM is not available (25). In our study, we report on the first 143 patients undergoing LAGB (see below).
Waist circumference (in centimeters) and waist to hip (W/H) ratio were evaluated, and an ultrasound (US; Ref. 26) and computerized tomography (CT) scan (27) evaluation of visceral and sc adipose tissue were performed (ultrasound thickness of visceral adipose tissue, ultrasound thickness of sc adipose tissue, CT scan thickness of visceral adipose tissue, CT scan thickness of sc adipose tissue, CT scan area of visceral adipose tissue, and CT scan area of sc adipose tissue). Eligible patients underwent a preliminary upper gastrointestinal tract evaluation by using x-ray and endoscopy; they were informed of all screening tests and procedures connected with LAGB and follow-up. At the end of the evaluation procedure, suitability for surgery was established by the internist and the surgeon, based on the results of the cardiologist and anesthesiologist visit and risk assessments. Patients also underwent a psychological and psychiatric evaluation, based on structured interviews followed by ad hoc scales of evaluation to exclude major psychiatric disorders (28, 29). The 143 eligible patients [27 men and 116 women; age, 42.9 ± 0.83 yr; BMI, 44.9 ± 0.53 kg/m2; classified at OGTT as normal glucose tolerance (NGT; n = 77), IGT (n = 47), or T2DM (n = 19)] underwent LAGB. After surgical procedure (Ref. 22 ; all procedures were performed by M.P. and M.G., two staff senior surgeons) they were reevaluated by the dietitian and a physician at fortnight intervals for 2 months and then monthly up to 1 yr. For the first month after LAGB, a semiliquid diet of 800 and 950 kcal/d in women and men, respectively, was prescribed (33% proteins, 19% lipids, 48% carbohydrates).
Patients were advised to eat slowly, to avoid liquids during meals, to use vegetables at each meal and meat or fish at least once a day, and to stop eating when feeling a sense of satiety. One month after LAGB, a solid diet was reintroduced, and by the third month the suggested diet was 970 and 1090 kcal/d in women and men, respectively; iron was supplemented on the basis of blood examinations performed during the second month. Diet included 48% carbohydrates (starch or bread), 33% proteins (fat free parts of different animals and fishes), and 19% lipids (olive oil); sweets, cakes, sweetened drinks, alcohol, and animal lipids were forbidden. All foods had to be cooked without oil, butter, or other lipids. Once or twice weekly, eggs or lean Parma ham or ricotta cheese were allowed in proper quantities. Diets were given by a dietitian and a physician with a specific training in obesity treatment and nutrition. The patients were also suggested to take 30-min physical aerobic activity every day to avoid muscular loss, with a gradual increase over a 1-month period. Physical activity could be gymnastics, swimming, or also dancing. Patients were instructed to eat only allowed nutrients and to keep a record of ingested foods, physical activity, and problems encountered.
Patients were scheduled for further assessment at 3-month intervals for 1 yr and at 6-month intervals thereafter. The public Italian health system fully covers the cost of this procedure. We have made a detailed cost analysis of the procedure, including hospital stays and follow-up visits, and the total cost is 10,850 euro or 10,000 U.S. dollars.
Diet-treated patients
Because it is unethical to perform sham operations in humans, we ruled out the possibility of a randomized study. To compare the LAGB effects with standard diet treatment, we identified 120 obese patients with similar clinical and metabolic characteristics (51 men and 69 women; age, 42.9 ± 1.11 yr; BMI, 43.6 ± 0.46 kg/m2; NGT, 66 patients; IGT, 8 patients; T2DM, 46 patients) who were regularly attending the obesity and diabetes outpatient clinics. Patients were evaluated under basal conditions and at 3-month intervals for 1 yr (measurement of body weight and assessment of food intake through review of diet diaries) and received standard care (education on eating behaviors, advice on diet and exercise). Their diet was between 1000 and 1200 kcal/d for women and men (22% protein, 29% lipids, and 49% carbohydrates).
Outcome measures
Clinical and metabolic effects of LAGB. Obese patients were evaluated at baseline and after 1, 2, and 3 yr for BMI, waist circumference, W/H ratio, arterial blood pressure, glycosylated hemoglobin (1c), fasting glucose and insulin levels, triglycerides, cholesterol (total cholesterol, high-density lipoprotein (HDL)-cholesterol, and total/HDL cholesterol ratio), uric acid levels, and homeostasis model assessment (HOMA; Ref. 30); aspartate aminotransferase (AST) and alanine aminotransferase (ALT) were used as an index of liver steatosis (31). OGTT was repeated in all subjects with an evaluation of glucose and insulin levels. These changes were also evaluated as a function of initial glucose tolerance (NGT, IGT, T2DM) and as a function of the amount of weight loss.
Detailed evaluation of body fat distribution. In addition to waist circumference and W/H ratio, US and CT scan evaluation of visceral and sc fat were repeated in obese subjects 1 yr after LAGB.
Comparison with diet-treated patients. During the 1-yr follow-up, obese LAGB-treated patients and obese diet-treated patients were divided into quartiles of weight loss; then patients of the first and fourth quartiles in each group were compared in terms of metabolic changes.
Laboratory assays
Blood glucose (BG) levels were measured by a glucose-oxidase method (YSI, Inc., Yellow Springs, OH). Triglyceride levels were assayed by an enzymatic technique on a Cobas Fara II Centrifugal Analyser (Cobas Fara II, Roche, Basel, Switzerland; Ref. 32). Triglyceride intra-assay coefficient of variation (CV) was 1.7%, and the interassay CV was 3.4%. Total cholesterol and HDL-cholesterol levels were assayed by enzymatic automated spectro-photometric methods with a Cobas Fara II, with an intra-assay CV of 4.3% and an interassay CV of 8.8%. HbA1c was assayed by a routine HPLC method (33). Insulin was assayed by a Microparticle Enzyme Immunoassay (IMX, Abbott Laboratories, Abbott Park, IL) with a monoclonal antibody without cross-reactivity with human pro-insulin. Uric acid levels, AST, and ALT were analyzed by routine laboratory methods.
Calculations and statistical analysis
Values are expressed as mean ± SE, or as frequencies. Intrasubject changes were analyzed by a t test. Intergroup differences were analyzed by one-way factorial ANOVA followed by Scheffè’s multiple comparison test. P levels less than 0.05 were considered statistically significant.
Results
Surgical outcome and complications
The procedure was laparoscopic in 143 patients and laparotomic in 1 patient. Four procedures were converted to laparotomic technique, two because of conspicuous hepatomegaly and two because of gastric lesion seen immediately during retrogastric tunnelling. Another patient with an intraoperative gastric lesion had a sepsis, requiring removal of gastric banding on the postoperative day and is not considered in this report. Postoperative hospital stay was 7 d after laparotomy (1 patient) and 2.2 + 0.11 d after laparoscopy (143 patients). Overall mean postoperative hospital stay was 2.3 + 0.08 d. At the end of the surgical procedure, the gastric banding was left completely open, and therefore the first regulation was narrowing of the stoma. Eighty-eight patients (61.5%) required stoma regulation, due to loss of satiety and unsatisfactory weight loss despite reported strict adherence to dietary prescriptions. Banding regulation was considered feasible at least 3 months after its placement. In more detail, 88 patients required stoma regulation. Fifty-seven patients underwent one regulation, 18 patients required two regulations (in 9 patients the second regulation was widening of the stoma), 12 patients required three regulations (in 8 patients, one widening), and 1 patient required six regulations. Thus, a total of 135 regulation procedures were performed under radiological control. Long-term complications included four disconnections of the sc port that were corrected under local anesthesia and eight gastric slippages requiring reintervention (laparotomic in one case and laparoscopic in seven cases) to replace the band with a new one (complication rate, 8.3%). Figure 1
shows the contrast x-ray of the stomach 1 d after the application of LAGB.
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Table 1 shows BMI, waist circumference, W/H ratio, arterial blood pressure, and metabolic variables in the group of 143 patients followed up for 3 yr. BMI changed from 44.9 ± 0.53 kg/m2 to an average value of 37 kg/m2. All values significantly improved compared with baseline, although a slight nonsignificant rebound at 3 yr for fasting glucose, insulin levels, and HOMA was observed as well as a continuous decrease in diastolic blood pressure, uric acid, and HbA1c; the number of patients with IGT or T2DM also declined significantly.
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shows that improvements in HbA1c, fasting BG, HOMA, HDL-cholesterol, and triglycerides were more evident in T2DM than in IGT or NGT subjects, so that at 3 yr HbA1c, HOMA, HDL-cholesterol, and triglycerides were not different in the three groups. The amount of weight loss was similar in the three groups.
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Table 2 shows detailed evaluation of body fat distribution (waist circumference, W/H ratio, CT, and US evaluation) at baseline and 1 yr after LAGB. All means of body fat distribution unanimously indicated a greater change of visceral fat than of sc fat. All changes, in addition, correlated with the amount of weight loss (data not shown).
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shows BMI in LAGB-treated patients and in diet-treated patients, the latter being followed up for 1 yr. BMI similarly decreased in the two groups of patients up to 6 months, re-increasing to basal level after 1 yr in diet-treated patients, while persisting for the duration of the 3-yr follow-up in LAGB-treated patients.
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compares metabolic changes in LAGB-treated patients and diet-treated patients, divided according to quartiles of weight loss. LAGB-treated patients (first quartile) and diet-treated patients (fourth quartile) had a similar weight loss; in these patients, metabolic changes were minimal and similar; in contrast, several metabolic changes were significantly different within LAGB-treated patients, and within diet-treated patients, divided according to quartiles of weight loss.
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In this study, we found that LAGB induced a significant reduction of body weight, accompanied by improvement of arterial blood pressure, glucose and lipid metabolism, and reduction of transaminases, which indicates reduction of liver steatosis (29). The clinical and metabolic effects described here are in line with the results obtained by gastric bypass, an invasive, not reversible approach (17).
LAGB induced a decrease of several risk factors for cardiovascular disease, yielding a lower arterial blood pressure and a less atherogenic profile (decreased uric acid and triglycerides, BG, insulin, and HOMA, increased HDL-cholesterol levels); in summary, the significant reduction of body weight was able to address several features of the so-called metabolic syndrome (34, 35). Our data also show that weight loss induced by LAGB is associated with a significant decrease of visceral and sc adipose tissue and with a greater loss of visceral fat than of sc fat, and it is accepted that visceral fat mediates most of the metabolic consequences of obesity (36).
The effects of LAGB were more evident in T2DM than in IGT and NGT subjects. It is interesting to note that despite similar weight loss, the greatest reduction in HbA1c, fasting BG, HOMA, and triglycerides occurred in T2DM, and the greatest increase in HDL-cholesterol also occurred in T2DM, so that in 3 yr HbA1c, HOMA, HDL-cholesterol, and triglycerides were similar in NGT, IGT, and T2DM subjects.
Trying to identify reasons for these results, the above data were analyzed as a function of quartiles of weight loss. Behavior of patients was consistent throughout the entire follow-up period, about half of the patients (first and second quartiles) had a modest although statistically significant weight loss, followed by a trend toward regain of body weight; the third quartile had a stable reduction of BMI, and the fourth quartile showed a steady decline of BMI. We found that patients with lower BMI (first and second quartiles, 42.2 ± 0.73 and 43.8 ± 0.97 kg/m2, respectively) were the ones who benefited less from the procedure, reaching at 3 yr 38.3 ± 1.94 and 39.2 ± 2.37 kg/m2, respectively (both P < 0.05); patients with higher BMI at recruitment (third and fourth quartiles, 44.1 ± 0.76 and 49.8 ± 1.29 kg/m2, respectively), were the ones to benefit more from the procedure reaching after 3 yr 35.8 + 1.55 and 37.4 + 1.93 kg/m2, respectively (P < 0.001 and P = 0.0001). Thus, although all patients benefited in a statistically significant way from the procedure, reaching BMI 36 to 39 kg/m2, heavier patients will benefit from the procedure more, in terms of both relative and absolute BMI drop. The rate of success did not change over the years. Also, patients with lower compliance to scheduled visits reported more problems with dietary instructions and had a worse outcome than patients with a better compliance and fewer problems. By comparing the first and fourth quartiles, it appeared that the amount of weight loss was significantly associated with reduced waist circumference and W/H ratio at all time intervals, and with improvement of some metabolic variables at either 1, 2, or 3 yr.
Also, body fat distribution, evaluated through CT and US abdominal scanning at 1 yr, was proportional to the amount of weight loss.
Therefore, these data indicate that clinical and metabolic effects are proportional to the amount of weight loss, suggesting that the amount of weight loss is crucial in improving long-term prognosis in grade 3 obesity. This finding is consistent with epidemiological data indicating that the rate of diabetes decreases linearly with the amount of weight loss (37).
The importance of the amount of weight loss in determining metabolic improvements is also supported by the 1-yr comparison with diet-treated patients. The average weight loss was significantly greater in LAGB-treated patients than in diet-treated patients, so that the first quartile of LAGB-treated patients and the fourth quartile of diet-treated patients had a similar weight loss; in these two groups of patients, metabolic changes were similar and of modest entity. As repeatedly reported in the literature (38), diet-treated patients experienced a transitory, although significant, weight loss followed by relapse.
To our knowledge, this is the first study in which the effect of bariatric surgery on weight loss is compared with medical dietary treatment of grade 3 obesity at a single institution. However, these data should be interpreted with caution, because the study was not randomized, patients undergoing LAGB had a more intensive schedule of visits during the follow-up than control patients, and the value of intensive schedules of control has been proven in studies concerning obesity (38), T2DM (39, 40), T1DM (41), and arterial hypertension (42, 43).
One concern about LAGB is that its effects may not last indefinitely. Our follow-up data during the second and third years indicate that after the first year BMI plateaus, with no significant regain in BMI, whereas improvements in glucose and lipid metabolism are maintained or continued. This durable effect on glucose metabolism is promising, because the United Kingdom Prospective Diabetes Study 34 demonstrated that in overweight diabetic patients improvement of glucose metabolism obtained through metformin is accompanied by a reduction of the risk for cardiovascular disease (40). It may be possible to increase the effects of LAGB when BMI remains in the pathological range even 3 yr after LAGB, by the addition of drugs reducing appetite (sibutramine; Ref. 44), decreasing fat absorption (metformin and orlistat), or blocking insulin release (diazoxide) (45).
Glucose tolerance improved during the 3 yr of follow-up and is consistent with data obtained through gastric bypass (18), which indicates that bariatric surgery is effective in the long run in reducing the number of patients affected by T2DM (17). The Swedish obesity study, an ongoing project consisting of a registry and an intervention study, employs gastric bypass, vertical banded gastroplasty, and gastric banding (46); it reported a lower incidence of diabetes in surgically treated patients than in controls from 480 health care centers in Sweden; unfortunately, these results, although in the same direction, are not comparable to the present data or to the data by Long et al. (18), because the diagnosis of diabetes is based only on self-reported data collected in questionnaires.
In conclusion, LAGB appears to be an effective treatment of grade 3 obesity in inducing long-lasting reduction of body weight and arterial blood pressure, modifying body fat distribution, and improving glucose and lipid metabolism up to 3 yr. An extended follow-up is under way to fully understand the effect of LAGB in the prevention and cure of T2DM and of associated cardiovascular diseases in patients with grade 3 obesity.
Acknowledgments
We acknowledge the excellent help of M. Fiorilli, Servizio di Psicologia Clinica; C. Arancio and D. De Molfetta, Divisione di Psichiatria IV; and R. Mangili, Divisione di Medicina I, Instituto di Ricovero e Cura a Carattere Scientifico Ospedale San Raffaele (Milano, Italy).
Footnotes
Preliminary data of this study were presented in abstract form at the 36th Annual Meeting of the European Association for the Study of Diabetes, Jerusalem, Israel, September 17–21, 2000.
This work was partly supported by a grant from the Universiy of Milano (to M.G.). F.F. is supported by Ministero della Sanità (RF 2000).
Abbreviations: ALT, Alanine aminotransferase; AST, aspartate aminotransferase; BG, blood glucose; BMI, body mass index; CT, computerized tomography; CV, coefficient(s) of variation; HbA1c, glycosylated hemoglobin; HDL, high-density lipoprotein; HOMA, homeostasis model assessment; IGT, impaired glucose tolerance; LAGB, laparoscopic adjustable gastric banding; NGT, normal glucose tolerance; OGTT, oral glucose tolerance test; T2DM, type 2 diabetes mellitus; US, ultrasound; W/H, waist to hip.
Received January 28, 2002.
Accepted April 15, 2002.
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BMI, kg/m2) in patients with grade 3 obesity undergoing LAGB (n = 71) and in patients treated with conventional diet (n = 58)