Duodenal Switch

1998 Scopinaro Report

The entire contents of this page are used with permission, and are copyright ©1998 by Nicola Scopinaro, MD, et al, all rights reserved. Text, graphics, and HTML code are protected by US and International Copyright Laws, and may not be copied, reprinted, published, translated, hosted, or otherwise distributed by any means without explicit permission. Reprint requests should be directed to Nicola Scopinaro, MD, Istituto di Clinica Chirurgica dell'Università, Ospedale S. Martino, 16132 Genova, Italy.

BILIOPANCREATIC DIVERSION
Nicola Scopinaro, MD, Professor of Surgery
Gian Franco Adami, MD, Associate Professor of Surgery
Giuseppe M. Marinari, MD, Assistant Professor of Surgery
Ezio Gianetta, MD, Associate Professor of Surgery
Enrico Traverso, MD, Assistant Professor of Surgery
Daniele Friedman, MD, Assistant Professor of Surgery
Giovanni Camerini, MD, Assistant Professor of Surgery
Giorgio Baschieri, MD, Resident
Alessabdro Simonelli, MD, Resident
Department of Surgery, University of Genoa School of Medicine, Genoa, Italy

Reprint requests:
Nicola Scopinaro, MD
Istituto di Clinica Chirurgica dell'Università
Ospedale S. Martino
16132 Genova, Italy

Table of Contents:
Abstract
Introduction
Case Material
Eating Habits
Bowel Habits
Weight Loss
Weight Maintenance
Other Beneficial Effects
Nutrition
Aspecific Complications
Specific Late Complications
     Anemia
     Stomal ulcer
     Bone demineralization
     Neurologic complications
     Protein malnutrition
Minor Or Rare Late Complications
Late Mortality
Elongations And Restorations
Conclusions
References
 

ABSTRACT

Biliopancreatic diversion (BPD) has made reacceptable the malabsorptive approach to the surgical treatment of obesity. The procedure, in a series of 2241 patients operated on during a 21 years period, caused a mean permanent reduction of about 75% of the initial excess weight. The indefinite weight maintenance appears to be due to the existence of a threshold absorption capacity for fat and starch, and thus energy, while the weight loss is partly due to increased resting energy expenditure. Other beneficial effects, besides those consequent to weight loss and/or reduced nutrient absorption, included permanent normalization of serum glucose and cholesterol without any medication and on totally free diet in 100% of cases, both phenomena being due to a specific action of the operation. Operative mortality was less than 0.5%. Specific late complications included: anemia, less than 5% with adequate iron and/or folate supplementation; stomal ulcer, reduced to 3.2% by oral H2-blockers prophylaxis; bone demineralization, increasing up to the fourth year and tending to decrease thereafter, with need of calcium and vitamin D supplementation; neurological complications, totally avoidable by prompt vitamin B administration to patients at risk; protein malnutrition, which was reduced to a minimum of 3% with 1.3% recurrence, in exchange with a smaller weight loss, by adapting the volume of the gastric remnant and the length of the alimentary limb to the patient's individual characteristics. It is concluded that the correct use of BPD, based on the knowledge of its mechanisms of action, can make the procedure a very effective and safe one in all hands.

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INTRODUCTION

The high complication rate and the overall unsatisfactory weight loss results of jejunoileal bypass (JIB) led in the years around 1980 to general abandoning of malabsorption approach for obesity surgery, the gastric restriction procedures becoming the currently used ones. Besides its complications, essentially due to the indiscriminate malabsorption and to the harmful effects of the  long blind loop, the main problem with JIB is its narrow "therapeutic interval". In fact, the total length of the small bowel left in continuity is restrained within the range of 40 to 60 cm, a shorter or longer bypass resulting in life-threatening malabsorption or no weight reduction, respectively. On the other hand, the massive intestinal adaptation phenomena cause an increase of the absorptive surface leading out of the upper limits of the above range, with ensuing substantial recovery of energy absorption capacity. This, in addition to the frequent need of restoration for major complications, ends in a high rate of failure with weight regain (1,2).

Because of the absence of a blind loop and of the malabsorption essentially selective for fat and starch, biliopancreatic diversion (BPD) is free of the complications pertaining to JIB (3,4). Moreover, BPD has a very wide "therapeutic interval", since, by varying the length of the intestinal limbs, any degree of fat, starch and protein malabsorption can be created, thus adapting the procedure to the population's or even the patient's characteristics, in order to obtain the best possible weight loss results with the minimum of complications (5). This extreme flexibility also allows to neutralize the consequences of intestinal adaptation phenomena, which, on the other hand, are little effective in BPD. The qualities of BPD have gradually led to reacceptance of malabsorption as a surgical approach to obesity therapy, the procedure being increasingly used in all the Western World in its numberless possible versions.

Results and complications of BPD, after more than twenty years of clinical use, are well known by all bariatric surgeons. Therefore, the main purpose of this article is to describe the physiology of the operation, whose knowledge has considerably increased in the last years. The full understanding of the mechanisms of action of BPD is of paramount clinical importance, since it enables any surgeon to exploit the ductility of the procedure in order to adapt it to its particular patients' population.

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CASE MATERIAL

Of the total series of 2241 patients operated on since May 1976, 1356 (438 men and 918 women) underwent the present "ad hoc stomach" (AHS) type of BPD performed by the same surgical team between June 1984 and April 1997. Mean age was 37 years (11-70), mean weight 128 kg (73-236), and mean excess weight was 69 kg (20-156), corresponding to 117% (41-311) and to a mean BMI of 47 kg/m2 (29-87). Maximum follow-up was 155 months. Follow-up rate was 98%.

In the AHS BPD (Fig. 1) the gastric volume, which is the main determinant of the initial weight loss (temporary food intake limitation due to decrease of appetite and occurrence of postcibal syndrome), is adapted to the preoperative excess weight and to other individual characteristics (such as sex, age, eating habits, social-economical status and expected degree of compliance), with the aim of attaining in all cases the weight of maintenance around the end of the first postoperative year with the minimum of nutritional complications (6). Intestinal lengths, which determine energy absorption and thus the weight of stabilization and its indefinite maintenance, were adapted to the patient's characteristics only in the last five years (as described below).

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EATING HABITS

During the first postoperative months all patients undergoing BPD, due to the food stimulation of the ileum (7), have reduced appetite, and they have early satiety, occasionally in association with epigastric pain and/or vomiting. These symptoms characterize the postcibal syndrome and are caused by rapid gastric emptying with subsequent distention of the postanatomotic loop. All these symptoms, the more intense and lasting the smaller the gastric volume, rapidly regress with time, most likely due to intestinal adaptation. One year after operation the appetite and the eating capacity are fully restored and patients mean reported food intake is one and a half time as much as preoperatively, independently of gastric volume. Patients undergoing BPD must be aware that for the rest of their lives they will absorb minimal fat (8), little starch, sufficient protein (8,9), and nearly all mono and disaccharides, short-chain triglycerides, and alcohol (i.e., the energy content of sugar, fruit, sweets, soft drinks, milk, and alcoholic beverages). They must also understand that when their body weight will have reached the level of stabilization the intake of these aliments may be varied as needed for individual weight adjustments.  

Interestingly, the vasomotory phenomena characterizing the dumping syndrome are always absent after BPD, this indicating the lack in the ileum of the specific receptors and/or the vasoactive gut hormones which are thought to be implicated in the pathogenesis of d.s.

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BOWEL HABITS

After full resumption of food intake, BPD subjects generally have two to four daily bowel movements of soft stools. All have foul smelling stools, and most have flatulence. These phenomena, which can be reduced by modifying eating habits or by neomycin or metronidazole administration, tend to decrease with time along with a reduction of bowel movement frequency and an increase of stool consistency. Diarrhea usually appears only in the context of postcibal syndrome, and then it rapidly disappears, being practically absent by the fourth month (5).

The absence of diarrhea after BPD is easily explained considering that, unlike following JIB, the loss of bile salt into the colon was calibrated to about 750 mg/day by choosing the appropriate length for the common limb (8), and that, due to the lack of fat digestion, steatorrhea is essentially neutral, fecal pH resulting around 7. In fact, studies on intestinal transit time after BPD showed, in comparison with preoperatively, a transport speed decreased by 50% in the small bowel but unchanged in the large bowel (8), this being in keeping with the observed changes in gut hormones active on intestinal motility (10).

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WEIGHT LOSS

Weight reduction after AHS BPD, when expressed as percent loss of the initial excess weight (IEW%L), was 74±15 at 2 years (1284 cases), 75±15 at 4 years (1092 cases), 75±15 at 6 years (785 cases), 76±15 at 8 years (394 cases), 77±16 at 10 years (122 cases) and 78±17 at 12 years (58 cases), with no differences between "morbidly obeses" and "super obeses" (IEW >120%) (5).

As said above, the initial weight loss is determined by the temporary forced food limitation occurring immediately after operation. On the contrary, the weight of stabilization depends on the amount of daily energy absorption allowed by the BPD, as a consequence of a mechanism which acts permanently. As a rule, the operated patient fully recovers appetite and eating capacity before the weight of stabilization is attained, so that the final weight loss depends on the reduced energy intestinal absorption. The weight of stabilization is also greatly influenced by the gastric volume, most likely because a smaller stomach, resulting in a more rapid gastric emptying, accelerates intestinal transit, thus reducing absorption. 

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WEIGHT MAINTENANCE

The extraordinarily good weight maintenance that occurs after BPD is exemplified by a group of 40 subjects who underwent the original "half-half" (HH) type of operation, which differs from the present AHS type only in that the stomach is bigger and the alimentary limb is longer (11). Comprehensibly, the weight reduction was smaller, but the weight attained was strictly maintained up to the 18th year of follow-up (Fig. 2). It is noteworthy that these data are the only over 15-years results ever reported in obesity therapy.

Some clinical-statistical observations on the modalities of this very long term weight maintenance indicate that body weight after BPD is essentially independent of individual and interindividual variations of food intake. This prompted us to investigate the relationships between usual energy intake and energy intestinal absorption.

Fifteen subjects two to three years following BPD, that is with body weight steadily normalized on free diet, after keeping a seven-day alimentary diary, were hospitalized and kept during a six-day period on an isoenergetic isonitrogenic diet, individually elaborated as much as possible similar to the average daily intake of each subject for all nutrients. The apparent absorption (AA, intake minus fecal loss) of energy, fat, nitrogen and calcium was determined in the last three days. The absorption of alimentary protein, by administration of I-125 albumin with a 60 g protein meal, and the resting energy expenditure (REE), by indirect calorimetry, were also assessed. Results are reported in Table 1. The reliability of our data is confirmed by the observation that the difference between mean daily total absorbed energy and mean REE (1324, range 891-1751, kcal/day) was well compatible with the 24-hour diet- and exercise-induced thermogenesis in a hospitalized subject with comparable body weight. Fat and energy intake were not correlated with intestinal AA as absolute values, while a negative correlation was found between intake and intestinal AA as percent of the intake (Kendall rank test: fat p<.05, energy p<.02). This means that in BPD subjects an increase of energy intake results in an increase of percent energy malabsorption, so that the absolute amount of energy absorbed tends to remain constant in each subject. This phenomenon can be explained hypothesizing that: the BPD digestive-absorptive apparatus has a maximum transport capacity for fat and starch, and thus energy; consequently, all the energy intake that exceeds the maximum transport threshold is not absorbed; therefore, assuming that daily energy intake is largely higher than the aforementioned threshold, daily energy absorption is constant for each subject. In conclusion, the original intestinal lengths and gastric volume being equal, the interindividual variability of the weight of stabilization in BPD subjects is accounted for by interindividual differences of original energy intestinal absorption capacity per unit of surface, of intestinal adaptation phenomena, of intestinal transit time (which, besides gastric volume, can be influenced by the intake of fluids), of  simple sugar intake and of energy expenditure per unit of body mass, but in each BPD individual the weight of stabilization cannot be modified by any increase or decrease of fat-starch intake, provided that the intake is greater that the maximum transport threshold.

Table 1: Energy, fat, nitrogen and calcium intestinal apparent absorption in 15 subjects (3 men) with stable body weight 2-3 years after BPD (mean ± s.d. body weight: at the time of the operation 119 ± 24 kg; at the time of the study 75 ± 14 kg).

 

 

alimentary intake

fecal loss

apparent absorption

apparent absorption (%)

energy (kcal/24h)

mean

3070

1329

1741

58

 

range

1840-4060

210-2590

1012-2827

32-71

 

fat (g/24h)

mean

130

89

39

28

 

range

88-185

22-251

13-94

12-59

nitrogen (g/24h)

mean

27

12

15

57

 

range

15-48

2.5-36

6.7-20

25-82

calcium (mg/24h)

mean

1994

1443

551

26

 

range

1037-3979

453-2565

251-1414

-24-69

The above results were confirmed by an overfeeding study, where 10 long term BPD subjects kept a strictly stable body weight when fed 15 days their usual diet and 15 more days the same diet plus 2000 fat-starch kcal/day (Table 2).

Table 2: Overfeedingstudy in 10 subjects 3-9 years after BPD. Individual data of body weight (BW, kg) at the beginning of the study, after a 15 day period on usual food intake (mean: ~ 3800 kcal/day) and after a 15 day period of overfeeding (usual food intake plus 2000 fat/starch kcal/day).

subjects

initial BW

BW on usual
food intake

BW after
overfeeding

1

77.7

78.0

78.0

2

90.0

90.5

89.2

3

97.0

96.5

95.7

4

73.0

72.7

73.4

5

89.1

88.8

90.3

6

68.5

68.0

68.5

7

102.8

103.5

103.0

8

87.0

87.0

86.5

9

66.5

66.0

66.0

10

70.5

70.0

71.0

When the food limitation effect has subsided and appetite and food intake are fully restored, the daily amount of energy absorption allowed by the BPD remains then the only determinant of body weight. The latter must decrease until the consequent decrease of energy consumption leads to a total energy expenditure (TEE) equal to daily energy intestinal absorption. Now, if we consider that in our patients population mean preoperative TEE is about 2250 kcal/day, mean energy absorption is about 1750 kcal/day, and mean total energy consumption per kg of weight loss is not less that 15 kcal/day (12), it is evident that the difference between mean preoperative TEE and mean postoperative daily energy absorption cannot account for the mean weight lost at stabilization, corresponding to about 50 kg. Furthermore, all of the many obese women with a preoperative TEE smaller than 1750 kcal/day lost weight after BPD. Therefore, an increase of energy expenditure after BPD had to be hypothesized, already suggested by three previous studies (13,14,15) demonstrating following BPD an energy expenditure greater that what theoretically expected after the observed weight reduction.

A longitudinal study on REE in 53 subjects with stable preoperative body weight, prior to operation and one, two, and three years after BPD was then carried out, whose results are reported in Table 3. Though mean body weight had reduced by about 50 kg and mean lean body mass (LBM) by 8 kg,  mean REE at one, two and three years was very similar to the preoperative one. Since both preoperative and postoperative body weights were stable, and thus preoperative energy expenditure was equal to energy intake and postoperative energy expenditure was equal to energy absorption, postoperative energy absorption was equal to preoperative energy intake. In other words, on the average our subjects absorbed after BPD as much energy as they were eating before, and this rises obvious questions about the why of the weight loss.

Table 3: Body weight (BW, kg), body mass index (BMI, kg/m2), fat free mass (FFM, kg) and resting energy expenditure (REE, kcal/24h) in 53 obese subjects (11 men) prior to, one year, two years and three years after BPD, and in 30 never-obese healthy controls (mean ± s.d.).

 

BW

BMI

FFM

REE

prior to BPD

127.6 ± 26.9

47.4 ± 9.5

64.3 ± 12.9

1591 ± 638

at one year

83.0 ± 15.4 *

30.8 ± 5.6 *

55.5 ± 8.3 *

1578 ± 305

at two years

78.0 ± 12.6 *

28.9±4.4*

54.2 ± 8.6 *

1600 ± 310

at three years

79.4 ± 13.8 *

29.4 ± 4.8 *

55.8 ± 8.6 *

1580 ± 229

controls

77.2 ± 11.0*

28.5 ± 4.3*

53.9 ± 7.1 *

1317 ± 199

one-way ANOVA: * p < .0001 vs. preop.

The weight reduction in our sample can be explained considering the different energy expenditure of human body sectors. In fact, while adipose tissue consumes only about 5 kcal/kg/day (16), the REE of muscle is about 18 kcal/kg/day, and energy consumption of internal organs is as high as about 360 kcal/kg/day (17). Therefore, if energy intake remains constant, a relatively small variation in internal organ mass has to be balanced by a relatively great variation of the less consuming body sectors, namely adipose tissue and muscles, so that the overall energy expenditure, which must equal the energy intake, remains unchanged. Though plasma levels of the gut hormones that stimulate intestinal adaptation changes were found greatly increased after both JIB and BPD (10), after the latter, differently from what happens following JIB, the entire bowel receive the intraluminal stimulus to adaptation (18), and this causes an increase of size (Fig. 3 and 4) and functional activity of the whole intestinal tract (19,20). This obviously results in an increase of energy consumption, which, since the daily energy absorption cannot be modified, must be balanced by a loss of the other body sectors such as to produce an identical decrease of energy consumption, so that the eventual overall energy expenditure equals the energy intestinal absorption. Actually, the increase of energy expenditure attributable to the augmented bowel size-function fully accounts for the corresponding decrease due to the loss of adipose tissue, muscle mass and non-bowel visceral mass in our sample of operated patients (21).

Therefore, in our 53 BPD subjects, on the average the weight loss can be entirely explained by the changes of body composition that follow the operation. Anyway, the presence of a great interindividual variability suggests that very different situations may exist. On one extreme, to a great increase of bowel mass with a low energy transport threshold should correspond the maximum of weight loss, the minimum corresponding to the opposite case, with all the possible intermediate situations where the weight loss is mainly due either to the decreased energy absorption or to the increased energy expenditure. For example, if in our sample men and women are considered separately (Table 4), the striking fall of REE after BPD in men suggests that weight loss is mainly due to decreased energy intestinal absorption, while the significant increase of REE observed in women, in spite of a 43 kg reduction of body weight, clearly indicates that in the majority of cases the weight loss is entirely accounted for by the changes of lean body mass composition.

Table 4: Body weight (BW, kg), body mass index (BMI, kg/m2), fat free mass (FFM, kg) and resting energy expenditure (REE, kcal/24h) in obese subjects prior to, one year, two years and three years after BPD (mean ± s.d.).

 

BW

BMI

FFM

REE

men (11)

 

 

 

 

prior to BPD

147.8 ± 32.9

49.3 ± 11.5

76.9 ± 18.6

2128 ± 979

at one year

91.5 ± 17.1 *

30.4 ± 6.7 *

62.6 ± 11.6 †

1787 ± 346 §

at two years

83.4 ± 13.0 *

27.5 ± 4.0 *

62.0 ± 12.6 †

1752 ± 365 §

at three years

85.0 ± 13.2 *

28.0 ± 4.0 *

63.7 ± 9.9 †

1720 ± 251 §

 

 

 

 

 

women (42)

 

 

 

 

prior to BPD

120.5 ± 20.7

46.5 ± 8.8

60.1 ± 6.2

1425 ± 336

at one year

80.0 ± 13.7 *

30.8 ± 5.3 *

53.1 ± 5.0 *

1508 ± 254

at two years

76.2 ± 11.9 *

29.2 ± 4.5 *

52.5 ± 4.3 *

1546 ± 270 †

at three years

77.6 ± 13.6 *

29.8 ± 5.0 *

53.3 ± 6.3 *

1533 ±200 §

one-way ANOVA: § p < .05 vs. preop.
† p < .02 vs. preop.
* p < .0001 vs. preop.

In conclusion, after BPD the weight maintenance is ensured by the existence of an intestinal energy transport threshold, while the weight of stabilization depends partly on that threshold and partly on the changes of body composition consequent to the operation.

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OTHER BENEFICIAL EFFECTS

The other benefits obtained after BPD are listed in Table 5. The percentage of changes observed after the operation were calculated for each complication in patients with a minimum follow-up corresponding to the postoperative time after which there was generally no further substantial modification. Recovery and improvement were considered only when favorable changes were essentially maintained at all subsequent reexaminations. The observed beneficial effects are obviously not attributable to the BPD itself, but to the weight loss and/or the reduced nutrient absorption, the only two exceptions being the effects on glucose and cholesterol metabolism.

Table 5: Other beneficial effects of AHS BPD.

 

minimum
follow-up (mo)

disappeared (%)

improved (%)

unchanged (%)

impaired (%)

pickwickian syndrome* (2%)

1

100

-

-

-

somnolence† (6%)

1

100

-

-

-

hypertension‡ (39%)

12

81

13

6

-

fatty liver§ (46%)

24

87

9

4

-

leg stasis (31%)

12

45

39

16

-

hypercholesterolemia¶ (55%)

1

100

-

-

-

hypertriglyceridemia (33%)

12

95

5

-

-

hyperglycemia (14%)

4

100

-

-

-

diabetes mellitus (6%)

4

100

-

-

-

diabetes mellitus requiring insulin (2%)

12

100

-

-

-

hyperuricemia (16%)

4

94

-

3

3

gout (2%)

4

100#

-

-

-

(%) percent of patients with condition
* somnolence with cyanosis, polycythemia, and hypercapnia
† in absence of one or more characteristics of pickwickian syndrome
‡ systolic ³ 155, diastolic ³ 95 mm Hg, or both
§ more than 10%
 moderate or severe
¶ more than 200 mg/ml (22% more than 240 mg/ml)
# serum uric acid normalized, no more clinical symptoms

In fact, out of the 1773 (total series) AHS BPD patients with a minimum follow-up of one year, not only the 248 (14%) with preoperative simple hyperglycemia, nor only the 108 (6.1%) with type II diabetes mellitus manageable with oral hypoglycemics, but also the 32 (1.8%) patients with preoperative type II diabetes mellitus requiring insulin therapy, one year after BPD and permanently thereafter had normal serum glucose level without any medication and on totally free diet. Comprehensibly, this is accompanied by serum insulin levels normalization, as demonstrated by us in cross-sectional (22) and longitudinal (serum insulin in 53 AHS BPD subjects: preop. 18±10 mcU/ml; at 1 year 5.2±2.3; at 2 years 4.6±2.0; at 3 years 6.0±3.1; controls 6.9±2.6; ANOVA: each group vs. preop. <.0001) studies, as well as normalization of insulin-sensitivity (Table 6). Considering that about 20 percent of type II diabetes mellitus patients are not obese, and about 20 percent of formerly obese patients with type II diabetes mellitus still require insulin therapy after weight normalization by dieting, it must be concluded that simple weight loss or intraabdominal fat reduction cannot account for the observed 100 percent recovery from type II diabetes mellitus after BPD. Actually, our preoperatively diabetic patients had on the average normal serum glucose concentration already one month after operation, when the excess weight was still over 80%, this also indicating a specific action of BPD on glucose metabolism. The latter could be identified with the virtual annulment of the entero-insular axis. Indeed, serum GIP concentration shows after BPD a substantially flat curve in response to the test meal, along with normalization of basal and meal-stimulated serum insulin levels (10).

Table 6: Serum glucose and insulin concentrations and insulin sensitivity (euglycemic hyperinsulinemic clamp) in obese patients, in subjects 2-4 years after BPD and in lean controls.

 

 

obese subjects

BPD subjects

lean controls

No.

 

9

6

6

glycemia (mg/dl)

mean

99.1 *

74.6

86.6 *

 

range

63-116

69-81

83-92

insulinemia (mcU/ml)

mean

21.7

4.4 §

10.3 §

 

range

11-41

1-13

9-12

glucose uptake (mg/kg/min)

mean

2.9

9.3 †

10.5 †

 

range

1.7-7.2

6.8-11

8.5-12

U-Mann Whitney test:
* p < .01 vs. BPD subjects
§ p < .03 vs. obese patients
† p < .001 vs. obese patients

Another specific action of BPD accounts for the permanent serum cholesterol normalization in 100 percent of the operated patients, and it is the calibrated interruption of the entero-hepatic bile salt circulation, which cause an enhanced synthesis of bile acids at the expenses of the cholesterol pool. Serum cholesterol level shows a stable mean reduction of approximately 30% in patients with normal preoperative values and of 45% in patients who where hypercholesterolemic before the operation (23). High-density lipoprotein (HDL) cholesterol remains unchanged, the reduction being entirely at the expenses of low-density lipoprotein and very low-density lipoprotein cholesterol (24). These results were maintained at long term, the HDL cholesterol showing a significant increase, in 51 BPD subjects at 6 years (total serum cholesterol: preop. 210±46, postop. 124±25 mg/dl, Student's t test, p <.0001; HDL cholesterol: preop. 44±12, postop. 50±15 mg/dl, Student's t test, p <.03) and at very long term in the ten HH BPD subjects whose values were available 15-20 years after operation (Table 7). With the National Institutes of Health criterion of 200 mg/dl as the upper recommended limit for serum cholesterol, out of the total of 2229 (total series) obese patients submitted to BPD with a minimum follow-up of one month, 1226 had hypercholesterolemia (502 had values higher than 240 mg/dl, and 85 higher than 300 mg/dl). All of these patients had serum cholesterol values below 200 mg/dl one month after operation, and the values remained below that level at all subsequent examinations.

Table 7: Serum cholesterol (mg/dl) in ten subjects before and 15-20 years after HH BPD.

 

 

serum cholesterol 15-20 years after HH BPD

subjects

preoperative total serum cholesterol

total

HDL

1

205

116

47

2

140

125

38

3

150

140

52

4

210

158

65

5

280

158

73

6

230

127

61

7

180

118

35

8

285

120

36

9

189

130

59

10

260

171

33

mean

213

136 *

50

Wilcoxon test : p < .002 vs. preop.

Gasbarrini et al. (25.) submitted to HH BPD a lean young woman with familial chilomicronemia (serum triglycerides: 4500 mg/dl; serum cholesterol: 502 mg/dl) and type II diabetes mellitus (insulin 150 U/day to maintain serum glucose around 250 mg/dl). One year after operation she had gained 2 kg in weight, blood glucose was normal, serum triglycerides 380 mg/dl, serum cholesterol 137 mg/dl, on totally free diet and without any medication.

It is concluded that BPD may be effectively used for the treatment of severe type II diabetes mellitus and familial hyperlipidemia also in lean subjects.

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NUTRITION

The easiest way to appraise nutritional status is to observe and talk to the subject. A person who looks well and exhibits complete well-being and ability to work, generally has good nutritional status. This has been the case for nearly all the AHS BPD patients once the early postoperative period has passed. Our studies on particular aspects of nutritional status showed normal immunological status (26), physiological composition of the weight lost with attainment of a stable healthy body composition (27), and capacity of getting pregnant, carrying out a normal pregnancy and delivering healthy babies (28).

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ASPECIFIC COMPLICATIONS

The increasing practice and experience led us out of the learning curve with BPD as far as immediate complications are concerned. When the first 856 subjects, the subsequent 250 subjects, and the last 250 subjects undergoing AHS BPD are evaluated separately, a stable reduction of operative mortality to less than 0.5% and the near disappearance of general and intraabdominal complications are seen. Similarly, the incidence of wound complications appears to be steadily reduced to approximately 1% (Table 8).

Table 8: Immediate complications following biliopancreatic diversion.

 

first 856 subjects
June 1984-May 1991

next 250 subjects
May 1991-Feb. 1993

last 250 subjects
Feb. 1993-Apr. 1997

operative mortality

0.8%

3 heart arrest
2 pulmonary embolism
1 malignant hyperthermia
1 wound infection

0.4%

1 pulmonary embolism

0.4%

1 pulmonary
embolism

general complications

1.1%

5 pulmonary embolism
1 pneumonia
3 deep thrombophlebitis

-

0.4%

1 deep
thrombophlebitis

surgical complications

2.5%

2 GEA leak
1 gastric perforation
2 intraperitoneal bleeding
7 wound dehiscence
9 wound infection

1.6%

1 wound dehiscence
3 wound infection

1.2%

1 intraperitoneal bleeding
1 wound dehiscence
1 wound infection

On the contrary, the incidence of aspecific late complications, around 10% for incisional hernia (greater than 3 cm) and 1% for intestinal obstruction has not substantially changed through the years. Of note is the potential seriousness of the biliopancreatic limb obstruction, which, because of its particular anatomo-functional situation, does not cause any specific clinical or radiological signs. However, it may lead to acute pancreatitis, this being more probable and more rapid in onset when the obstruction is more proximal. Any acute abdominal pain that raises suspicion of this complication should lead to an immediate search for duodenal and proximal jejunal distention (by ultrasound scan) as well as testing for abnormally high levels of serum amylase and bilirubin. If one or more of these signs are present, immediate laparotomy is mandatory (29).

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SPECIFIC LATE COMPLICATIONS

Anemia

The exclusion of the primary site for iron absorption in the alimentary tract causes this unavoidable complication. More rarely, the anemia is due to folate deficiency and, exceptionally, to vitamin B12 deficiency. Anemia appears only in BPD patients with chronic physiologic (menstruation) or pathologic (hemorrhoids, stomal ulcer) bleeding. Reflecting the different causes for the anemia, most cases are microcytic, less are normocytic, and few are macrocytic. The general incidence of anemia after BPD in our population would probably be around 40%, but supplementation with periodic iron, folate, or both can reduce its occurrence to less than 5%. Over time, less supplementation is required.

Stomal ulcer

Stomal ulcer after BPD is more frequent in men, and its incidence is strongly influenced, especially in women, by alcohol and even more by cigarette consumption. Most stomal ulcers (67%) appear within the first postoperative year and the remainder by the second year. They respond well to medical treatment (94% healing with H2-blocker therapy) and have little tendency to recur, provided the patient refrains from smoking; thus they do not represent a long-term problem. Nevertheless, one fifth of ulcer healings occur with gastroenterostomy stenosis requiring endoscopic dilatation or surgical revision with higher gastrectomy.

The incidence of stomal ulcer was initially rather high (12.5% in the HH BPD), because of the great residual parietal cell mass. It was successively reduced to 8.3% in the initial group of patients submitted to AHS BPD (first 684 consecutive cases with a minimum follow-up of 2 years), simply due to the reduction of stomach size (30). Some changes of surgical technique, such as preserving as much as possible the gastrolienal ligament with its sympathetic nerve fibers (8), and shifting from end-to-end to end-to-side gastroenterostomy, the latter being better vascularized and less prone to stenosis (31), led to a further progressive reduction (5.6% in the subsequent 300 cases). In the last group of 300 AHS patients with minimum follow-up of 2 years, thanks to H2-blockers oral prophylaxis (32) during the first postoperative year in the patients at risk (started at the beginning of 1991), the incidence of stomal ulcer was ulteriorly reduced to 3.2%, with 44% occurrence in the second postoperative year.

Bone demineralization

The duodenum and proximal jejunum are selective sites for calcium absorption. However, the study on calcium intestinal absorption showed a more than sufficient apparent absorption in the 15 subjects on free diet (see Table 1). Moreover, intestinal absorption as absolute value were positively correlated with the intake (Kendall rank test: p <.03), what means that, unlike fat and energy, an increase of calcium intake results in an increase of absorption. Therefore, all of our patients are encouraged to maintain an oral calcium intake of 2 g/day (with tablets supplementation, if needed) and to receive a monthly intramuscular vitamin D supplementation of 400,000 IU.

The bone problems caused by BPD do not seem to differ substantially from those reported after distal gastrectomy with duodenal exclusion for peptic ulcer (33) and after gastric bypass for obesity (34). Histomorphologic signs of bone demineralization (cross-sectional study on 252 transiliac bone biopsies after double-labeling with tetracycline) were present in a little less than one third of the obese patients. Prevalence and severity of alterations increased after BPD until the fourth year (chi-square test: p<.001), at which point they tended to regress. Long-term (6-10 yr.) mineralization status was not significantly worse than that observed before operation. The patients with the most severe preoperative alterations, i.e. the older and the heavier, showed a sharp improvement in bone mineralization status as compared with preoperative status (prevalence of moderate to severe alterations in patients over 45 yr. old: preop. 25%, at 1-2 yr. 29%, at 3-5 yr. 33%, at 6-10 yr. 11%; in patients with IEW greater than 120%: preop. 24%, at 1-2 yr. 28%, at 3-5 yr. 53%, at 6-10 yr. 14%) (35, 36, 37).

Histomorphology data were in total agreement with clinical findings. Bone pain attributable to demineralization (with prompt regression after calcium and vitamin D therapy) was observed in 6% of patients, generally between the second and fifth postoperative years (maximum prevalence: 2.4% in the fourth year), and more rarely at long term (10-20 yr.) Three cases of rib fractures were reported so far in patients undergoing AHS BPD.

Neurologic complications

Peripheral neuropathy and Wernicke encephalopathy, early complications caused by excessive food limitation (38), have now totally disappeared (none in the last consecutive 1450 patients of the total series with a minimum follow-up of 1 year) because of prompt administration of large doses of thiamin to patients at risk, that is those reporting a very small food intake during the beginning postoperative weeks.

Protein malnutrition

Characterized by ipoalbuminemia, anemia, edema, asthenia, alopecia, protein malnutrition (PM) represents the most serious late specific complication of BPD, and its correction generally requires two to three weeks of parenteral feeding.

The understanding of the pathogenesis of PM following BPD has considerably improved during the last years. Protein intestinal absorption (by means of I-125 albumin)  had been investigated at the beginning of the clinical experimentation (9), and the study had been repeated after the completion of the developmental phase (39) with similar results. Still, the observed about 30% protein malabsorption did not seem to explain the occurrence of PM. A determinant contribution came from the more recent and complete study on intestinal absorption mentioned above. In fact, the comparison between alimentary protein intestinal absorption (73%) and nitrogen apparent absorption (see Table 1) revealed a mean loss of endogenous nitrogen of about 5 g/day, corresponding to protein about 30 g/day, that is approximately five-fold the normal value. Assuming as normal a 40 g/day protein requirement with a loss of about 6 g/day, all calculations made, the average  post-BPD protein requirement should be about 90 g/day, which is quite reasonable considering that the 15 long-term subjects in our study had an average intake of about 170 g/day.

The increased loss of endogenous nitrogen is of much greater importance in the first months following BPD, when the forced food limitation causes a negative balance both for energy and nitrogen, thus creating a condition of protein-energy malnutrition (PEM). In the latter, as it is known, two different subtypes can be identified: marasmic form (MF) and hypoalbuminemic form (HAF). In the MF PEM, which represents the effective metabolic adaptation to starvation, both energy and nitrogen deficits are present. The ensuing hypoinsulinemia allows lipolysis and proteolysis from skeletal muscles which supplies aminoacids for visceral pool preservation and hepatic synthesis of glucose, necessary for brain, heart and kidney metabolism and for the oxidation of fatty acids. This, in association with protein sparing due to energy negative balance, ensures both energy and protein homeostasis. The result is a loss of weight due to reduction of adipose tissue and muscle mass in complete well-being. On the contrary, in the HAF PEM the nitrogen deficit is associated with a normal or near-normal energy (carbohydrate) supply. This causes hyperinsulinemia, which inhibits both lipolysis and skeletal muscle proteolysis. Not being able to draw on its protein stores, and in absence of protein sparing, the organism reduces visceral protein synthesis, with consequent hypoalbuminemia, anemia, and immunodepression. The result is a severely ill person with body weight unchanged or increased, maintained adipose tissue size, and lean body composition pathologically altered for decrease of visceral cell mass and increase of extracellular water.

In the early post-BPD period the preservation of protein homeostasis, already threatened by the negative energy-protein balance due to the food limitation, is made more difficult by the presence of the increased endogenous nitrogen loss which has to be counterbalanced. If the operated patient devotes its reduced eating capacity mainly to protein-reach food, he compensates the loss and, like the starving individual, develops a MF PEM, which is the goal of the procedure. If, on the contrary, he eats mainly carbohydrates, the nitrogen loss makes the HAF PEM even more severe than kwashiorkor. Paradoxically, a starving patient is in a better metabolic situation, since he can draw on his protein store to try both to satisfy the requirement and to compensate the loss. Though this is rarely achieved, the occurring HAF PEM is milder than that of the carbohydrate-eater. Between the two extremes, HAF PEM of different severity can take place in the patients with mixed intake, depending on how much on one hand protein intake is smaller than protein loss, and on the other hand the relatively excessive energy intake prevents skeletal muscle proteolysis and protein sparing.

The presence of an increased endogenous nitrogen loss also explains late sporadic PM which may exceptionally occur at any distance from BPD in case of reduced food intake for any reason or of prolonged diarrhea due to aspecific enterocholitis. PM is usually more severe in the latter situation since, being the colon a site of protein digestion-absorption after BPD (9), protein absorption may result more affected than carbohydrate absorption.

The goal of treatment in early PM, when a significant excess of weight is still present, is to change PEM from HAF into MF, giving the patients the possibility of exploiting his energy and protein stores. This is easily obtained by annulling alimentary carbohydrate intake and, keeping into account protein intake, administering intravenously only aminoacids in amount certainly sufficient to compensate endogenous protein loss. On the contrary, therapy of late PM, when body weight is normal or near-normal, must be aimed at the disappearance of PEM and restoration of normal nutritional status, with parenteral feeding containing both nitrogen and energy necessary to restoration of aminoacid pool, re-establishment of anabolic condition and re-synthesis of deficient visceral protein.

The pathogenesis of PM after BPD is then multifactorial, depending on some operation-related variables (gastric volume, intestinal limb lengths, individual capacity of intestinal absorption and adaptation, amount of endogenous nitrogen loss) and some patient-related variables (customary eating habits, ability to adapt them to the requirements, social-economical status). In most cases PM is limited to a single episode occurring during the first or the second year, the patients-related factors being pre-eminent. The delayed appearance of sporadic PM (see above) is less and less frequent as time passes by (40). The operation-related factors are of greater importance in the recurrent form of PM, usually caused by excessive malabsorption and requiring elongation of the common limb, and, rarely, by an excess of duration of the food limitation mechanism (permanent decrease of appetite and occurrence of postcibal syndrome) which may require restoration of intestinal continuity (5, 41).

In a remote phase of BPD development, in the attempt of both accelerating and increasing the weight loss, we drastically reduced mean gastric volume to about 150 ml, obtaining, besides an excellent weight reduction (near 90% of the IEW at two years), a catastrophic about 30% incidence of PM with 10% recurrence rate. With the aim of decreasing PM incidence without losing the benefit of the small stomach, the gastric volume was adapted to the patient's initial EW. In fact, the original philosophy of the "ad hoc stomach" was to confine the risk of PM to those patients who required a greater weight loss. This resulted in a 15.1% incidence of PM with 6.8% recurrence, while the mean weight reduction remained at a very satisfactory 79% of the IEW (initial 192 AHS BPD patients with a minimum follow-up of two years), the higher weight of stabilization being evidently due to the larger mean stomach volume (about 350 ml) with the consequent slower intestinal transit and greater energy absorption.

Actually, despite the absence of a negative correlation between stomach volume and weight reducion, BPD patients with a more than 300 ml gastric remnant lose significantly less than those with a smaller stomach. Subsequently, the other patient-related variables were also taken into account in the choice of gastric volume, with the new rationale of allowing only the patients with the best individual characteristics to take the risk/benefit of a smaller stomach. This new policy, entailing an increase of mean gastric volume to about 400 ml,  led to a further reduction of PM incidence, which progressed with the progressive improvement in use and increase in number of the criteria for adapting the stomach volume to the patient's characteristics. In fact, in the subsequent 859 AHS BPD patients, the first 430 had a PM incidence of 12.6% with 5.3% recurrence, the IEW loss decreasing to 75%, while the second 429 had an  incidence of 7.0% with 2.6% recurrence, paid by an only 2% mean reduction of the IEW, decreased to 73%. At that point, the disappearance of the negative correlation between gastric volume and occurrence of PM meant that stomach size had no more influence on PM incidence. In order to ulteriorly reduce the incidence of this complication, still preserving the best possible weight loss, we decided then to increase intestinal absorption in the patients at risk. The majority of them, in our series, are in the southern Italian population, where the main energy source are carbohydrates, the compliance is smaller, and the financial status is lower. Actually, in the first sub-group mentioned above the incidence of PM was 8.3% with 4.3% recurrence in the 230 patients from northern Italy, and 17.5% with 6.5% recurrence in the 200 patients from southern Italy, while in the second sub-group the corresponding values were 4.1% with 1.4% in 221 patients, and 10.0% with 3.8% in 208 patients.

Starting from September 1992, our policy was to create a 200 cm alimentary limb (AL) in all patients from North, unless their individual characteristics were strongly negative, and a 300 cm AL in the patients from South, unless their individual characteristics were strongly positive, some patients in both groups having an intermediate length of 250 cm. In the 107 patients from North who have reached a minimum follow-up of two years (6 with a >200 cm AL) only one subject with 200 cm AL had an early sporadic PM (0.9%), while in the 123 from South (104 with a >200 cm AL) PM occurred in the early sporadic form in two cases with >200 cm AL and one case with 200 cm AL (2.4%), and in the recurrent form in two cases of the first group and one of the second (2.4%), the overall incidence in the whole population of 230 operated patients being 3.0%, with 1.3% recurrence. This excellent result, which essentially means the near disappearance of necessity of surgical revision, was, as expected, paid in terms of mean reduction of IEW, which dropped to a mean of 71% (73% in the 120 patients with 200 cm AL and 68% in the 110 with >200 cm AL), the patients from North losing 73% and those from South 69%.

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MINOR OR RARE LATE COMPLICATIONS 

In the 1284 AHS BPD patients with a minimum follow-up of two years the following minor or rare complications were observed or reported: 55 (4.3%) cases of impairment or appearance of hemorrhoids; 24 (1.9%) cases of anal rhagades; 5 (0.4%) cases of perianal abscess; 45 (3.5%) cases of acne; 7 (0.5%) cases of inguino-perineal furuncolosis; 37 (2.9%) cases of night blindness; 3 cases of lipothymias from hypoglycemia; 2 cases of transient dumping syndrome; 1 case of bypass arthritis; 1 case of gallstone ileus. These minor complications showed a decreasing incidence in our population of operated patients. Anyway, they occur more and more rarely as time passes by, and tend to disappear at long term.

Alitosis after BPD could be due either to food stagnation in a virtually achloridric stomach, which can be avoided by a correct execution of the gastroenterostomy, or to pulmonary expiration of ill-smelling substances resulting from malabsorption, the oral administration of pancreatic enzymes being of use in these cases. This unpleasant side-effect has also become less and less common in our series, affecting today not more than 5% of the operated patients.

BPD causes oxalate hyperabsorption, but not hyperoxaluria, though the oxalate urinary excretion in the operated patients is significantly higher than in controls (42). The procedure can then be considered a remote cause of kidney stone formation, keeping in mind that not even hyperoxaluria can cause this complication in absence of co-factors, first of which decreased urinary volume from dehydration. The incidence of kidney stones in our series (5/1284 or 0.4%) does not differ from that of the general population. Thirty-two needle kidney biopsies taken at long term relaparotomies in BPD patients failed to demonstrate any microscopic or ultrastructural alterations (personal unpublished data: study in cooperation with Dr. Thomas Stanley, VA Hospital, Los Angeles, California, 1984).

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LATE MORTALITY

Specific late mortality consisted of three cases of protein malnutrition (inadequately treated elsewhere) and one case of Wernicke encephalopathy. Semispecific mortality (i.e., the operation acting as a remote cause of death) included three cases of alcoholic cirrhosis (the pharmacological effect of alcohol is enhanced by the distal gastrectomy due to more rapid intestinal absorption) and three cases of obstruction of the biliopancreatic limb (late or no diagnosis elsewhere). Eleven deaths were of unknown causes or were unrelated to BPD.

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ELONGATIONS AND RESTORATIONS

With the exception of seven cases of restoration of intestinal continuity for different reasons (four cases of alcoholic or posthepatitic symptomatic cirrhosis, two cases of psychologic intolerance of the environmental problems due to changed body shape, and one case of intolerance of intestinal gas problems), surgical revision of BPD was always required for recurrent protein malnutrition (5). Consequently, as said above, the fall of such complication to the present almost negligible incidence caused in our hands the near disappearance of the need of these specific reoperations.

It is very important to remember that, while fat should be essentially absorbed in the common limb, the protein and starch digestion/absorption capacity per unit of length of the common limb does not seem to be greater than that of the alimentary limb (44), so that protein absorption after BPD substantially depends on the total intestinal length from the gastroenteroanastomosis to the ileocecal valve. Therefore, the elongation of the common limb for correction of a recurrent protein malnutrition would be ineffective if done along the alimentary limb. The elongation must be performed at the expenses of the biliopancreatic limb, the length which in our experience has proven effective in all cases being 150 cm, with the result of a total of 400 cm of small bowel in the food stream.

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CONCLUSIONS

The studies carried out in the last years have greatly enlarged our knowledge on the physiology of BPD, and this has enabled us to make a better use of the procedure, thus improving considerably its cost/benefit ratio.

Biliopancreatic diversion is unanimously considered the most effective procedure for the surgical treatment of obesity. Like any other powerful weapon, it can be very dangerous if used improperly. Twenty years of careful investigation and clinical experience made it, in our hands, also a very safe remedy. It was a very long "learning curve", consisting essentially of adapting more and more the operation to the patient's individual characteristics, so that the best weight loss results be reserved to the subjects who are at low risk of nutritional complications, accepting a smaller weight reduction in the less compliant patients in order to minimize the potential nutritional problems. Our criteria of assessment are based on our personal experience with our cohort of patients, and therefore they are largely subjective; on the other hand, to try to standardize them would be of little use when dealing with a different population. All surgeons willing to obtain the best results with BPD should follow our example, finding the criteria to be used to adapt the operation to the patients in their population according to their individual characteristics. The ductility of the procedure is such that, theoretically, for each individual patient the best combination of stomach volume and intestinal lengths could be identified. Obviously, the adaptation must be based on the profound knowledge of all the mechanisms of action of BPD, which are today sufficiently known to allow any good will surgeon to obtain the best results at the lowest price in all patients.

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REFERENCES

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9) Bonalumi U., Cafiero F., Caponnetto A., Gianetta E., Reboa G., Civalleri D., Piccardo A., Berti Riboli E., Scopinaro N.: Protein absorption studies in biliopancreatic bypass patients. Int. J. Obesity 5: 543, 1981.

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13) Adami G.F., Campostano A., Bessarione D., Gandolfo P., Marinari G., Lamedica G., Scopinaro N.: Resting energy expenditure in long-term postobese subjects after weight normalization by dieting or biliopancreatic diversion. Obes. Surg. 3: 397, 1993.

14) Greco A.V., Tataranni P.A., Tacchino R.M., Caradonna P., Mingrone G., Raguso C., Castagneto P.: Daily energy expenditure in postobese patients. Int. J. Obesity 17: 27, 1993.

15) Marinari G., Simonelli A., Friedman D., Baschieri-Novelli G., Colombini M., Scopinaro N.: Very long-term assessment of subjects with "half-half" biliopancreatic diversion. Obes. Surg. 5: 124, 1995.

16) Nelson K.M., Weinsier R.L., Long C.L., Schutz Y.: Prediction of resting energy expenditure from fat-free mass and fat mass. Amer. J. Clin. Nutr. 56: 848, 1992.

17) Holliday M.A.: Metabolic rate and organ size during growth from infancy to adolescence and during late gestation and early infancy. Pediatrics 47: 101, 1971.

18) Dowling R.H.: Small bowel adaptation and its regulation. Scand. J. Gastroenterol.(suppl.) 74: 53, 1982.

19) Stock-Damgé C., Aprahamian M., Raul F., Marescaux J., Scopinaro N.: Small intestinal and colonic changes after biliopancreatic bypass for morbid obesity. Scand. J. Gastroenterol. 21: 1115, 1986.

20) Evrard S., Aprahamian M., Hoeltzel A., Vasilescu M., Marescaux J., Damgé C.: Trophic and enzymatic adaptation of the intestine to biliopancreatcic bypass in the rat. Int. J. Obesity 17: 541, 1993.

21) Scopinaro N., Gianetta E., Adami G.F., Friedman D., Traverso E., Marinari G., Camerini G., Vitale B., Baschieri G., Simonelli A., Gandolfo P., Bachi V.: Recenti acquisizioni fisiopatologiche e nuove strategie d'uso nella diversione biliopancreatica. Proceedings of the "Novantottesimo Congresso della Società Italiana di Chirurgia", Rome, October, 13-16, 1966; 2: 37-62.

22) Scopinaro N., Sarson D., L., Civalleri D., Gianetta E., Bonalumi U., Friedman D., Bloom S.R.: Changes in plasma gut hormones after biliopancreatic bypass for obesity. A preliminary report. Ital. J. Gastrenterol. 12: 93, 1980.

23) Gianetta E., Friedman D., Adami G.F., Traverso E., Castagnola M., Scopinaro N.: Effects of biliopancreatic bypass on hypercholesterolemia and hypertriglyceridemia. Proceedings of the Second Annual Meeting of the American Society for Bariatric Surgery, Iowa City, Iowa, June 13-14, 1985, pp. 138-142.

24) Montagna G, Gianetta E., Elicio N., Valice S., Degli Innocenti L., Marcenaro A., Scopinaro N., Bertolini S.: Plasma lipid and apoprotein pattern in patients with morbid obesity before and after biliopancreatic bypass. Atheroscl. Cardiovasc. Dis. 3: 1069, 1987.

25) Gasbarrini G., Mingrone G., Greco A.V., Castagneto M.: An 18-year-old woman with familial chylomicronaemia who would not stick to a diet. Lancet 348: 794, 1996.

26) Adami G.F., Civalleri D., Gianetta E., Friedman D., Scopinaro N.: In vivo evaluation of immunological status after biliopancreatic bypass for obesity. Int. J. Obesity 9: 171, 1985.

27) Adami G.F., Barreca A., Gianetta E., Friedman D., Traverso E., Castagnola M., Vitale B., Summa M., Semino G., Marinari G., Scopinaro N.: Body composition in subjects with surgically obtained stable body weight normalization. Int. J. Obesity 13: 55, 1989.

28) Friedman D., Cuneo S., Valenzano M., Marinari G.M., Adami G.F., Gianetta E., Traverso E., Scopinaro N.: Pregnancies in an 18-year follow-up after biliopancreatic diversion. Obes. Surg. 5: 308, 1995.

29) Gianetta E., Friedman D., Traverso E., Adami G.F., Vitale B., Marinari G., Cuneo S., Colombini M., Ballari F., Abbondati A., Scopinaro N.: Small bowel obstruction after biliopancreatic diversion. Problems in General Surgery 9:386, 1992.

30) Civalleri D., Gianetta E., Friedman D., Castagnola M., Simoni G., De Cian F., Repetto M., Scopinaro N.: Changes of gastric acid secretion after partial biliopancreatic bypass. Clin. Nutr. 5 (suppl): 215, 1986.

31) Gianetta E., Friedman D., Adami G.F., Traverso E., Vitale B., Semino G., Castagnola M., Summa M., Scopinaro N.: Present status of biliopancreatic diversion (BPD). Proceedings of the Third International Symposium on Obesity Surgery, Genoa, Italy, September, 20-23, 1987; pp. 11-13.

32) Adami G.F., Gandolfo P., Esposito M., Scopinaro N.: Orally-administered serum ranitidine concentration after biliopancreatic diversion. Obes. Surg. 1: 293, 1991.

33) Fisher A.B.: Twenty-five years after Billroth II gastrectomy for duodenal ulcer. World J. Surg. 8: 293, 1984.

34) Crowley L.V., Seay J., Mullin G.T. Jr.: Long term hematopoietic and skeletal effects of gastric bypass. Clin. Nutr. 5 (suppl): 185, 1986.

35)  Compston J.E., Vedi S., Gianetta E., Watson G.J., Civalleri D., Scopinaro N.: Bone histomorphometry and vitamin D status after biliopancreatic bypass for obesity. Gastroenterology 87: 350, 1984.

36)  Compston J.E., Vedi S., Watson G.J., Quiney J., Gianetta E., Friedman D., Scopinaro N.: Metabolic bone disease in patients with biliopancreatic bypass. Clin. Nutr. 5 (suppl): 221, 1986.

37) Adami G.F., Compston J.E., Gianetta E., Friedman D., Traverso E., Vitale B., Summa M., Camerini G., Scopinaro N.: Changes in bone histomorphometry following biliopancreatic diversion. Proceedings of the III International Symposium on Obesity Surgery, Genoa, Italy, September, 20-23, 1987; pp. 46-47.

38) Primavera A., Schenone A., Simonetti S., Gianetta E., Semino G., Scopinaro N.: Neurological disorders following biliopancreatic diversion. Proceedings of the Third International Symposium on Obesity Surgery, Genoa, Italy, September, 20-23, 1987, pp. 48-49.

39) Friedman D., Caponnetto A., Gianetta E., Adami G.F., Traverso E., Vitale B., Castagnola M., Semino G., Camerini G., Scopinaro N.: Protein absorption (PA) and protein malnutrition (PM) after biliopancreatic diversion (BPD). Proceedings of the Third International Symposium on Obesity Surgery, Genoa, Italy, September, 20-23, 1987, pp. 50-51.

40) Gianetta E., Friedman D., Adami G.F., Vitale B., Traverso E., Castagnola M., Semino G., Scopinaro N.: Etiological factors of protein malnutrition after biliopancreatic diversion. Gastroenterol. Clin. North Amer. 16: 503, 1987.

41) Scopinaro N., Gianetta E., Friedman D., Adami G.F., Traverso E., Vitale B., Castagnola M., Semino G., Summa M., Bachi V.: Surgical revision of biliopancreatic bypass. Gastroenterol. Clin. North Amer. 16: 529, 1987.

42) Hofmann A.F., Schnuck G., Scopinaro N., Laker M.F., Sherr H.P., Lorenzo D., Meeuse B.J.D.: Hyperoxaluria associated with intestinal bypass surgery for morbid obesity: occurrence, pathogenesis and approaches to treatment. Int. J. Obesity 5: 513, 1981.

43) Scopinaro N., Marinari G.M., Gianetta E., Adami GF., Friedman D., Traverso E., Camerini G., Baschieri G., Vitale P., Gandolfo P., Simonelli A.: The respective importance of the alimentary limb (AL) and the common limb (CL) in Protein absorption (PA) after BPD. Obes. Surg. 7:108, 1977.

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FIGURES (not shown)

Figure 1 (not shown): Schematic representation of AHS BPD. Alimentary limb, from gastroenterostomy to enteroenterostomy (EEA); biliopancreatic limb, from duodenum to EEA; common limb, from EEA to ileocecal valve.

Figure 2 (not shown): Changes of body weight after "half-half" BPD.

Figure 3 (not shown): The end-to-side enteroenterostomy two years after BPD. On the left the alimentary limb, in the middle the biliopancreatic limb, on the right the common limb.

Figure 4 (not shown): Same case as in Fig. 4. On the left the alimentary limb immediately distal to the GEA; on the right the biliopancreatic limb immediately distal to the ligament of Treitz.

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