Rarely, *diarrhea* is due to excessive reduction of ileal bile salt absorption. This condition can be easily diagnosed by cholestyramine administration, and it represents the only indication to the elongation of the CL along the alimentary one, 100 cm being sufficient in our experience (Fig. 6).

Restoration of the intestinal continuity is specifically indicated in presence of a recurrent PM and/or an excessive weight loss due to permanence of the food limitation effect with or without poor protein intake. The goal in these cases is to restore a normal intestinal absorption capacity in a subject who will maintain his/her weight reduction because of the permanently reduced food intake. This can be obtained with different operations, ranging from a simple high side-to-side enteroenterostomy to the complete reconstruction of the gastrointestinal tract, with a 50-cm ileal loop being interposed between the stomach and the duodenum (Fig. 7).

BPD and BPD-DS Concerns and Results 199

Fig. 8. Restoration bringing the AL to the ligament of Treitz.

Fig. 9. Restoration bringing the AL to the duodenum.

Restoration may be necessary if **a disease occurs whose consequences would be worsened by malabsorption**, e.g., liver cirrhosis, nephrotic syndrome, chronic inflammatory bowel disease, malignancy, or psychosis. It may also be requested by the BPD subject instead of the elongation after a long period of recurrent PM, or for different reasons, e.g., intolerance of the stool/gas problems, or psychological intolerance of the environmental problems

Fig. 6. Elongation of the CL along the AL.

Fig. 7. Full restoration of intestinal continuity.

We prefer to section the alimentary limb (AL) immediately proximal to the enteroenterostomy (EEA) and join the ileal stump to the jejunum, immediately distal to the ligament of Treitz. This type of restoration allows the resumption of a normal proteinenergy absorption, still partially preserving both the specific effects of BPD on glucose and cholesterol metabolism (Fig. 8).

Fig. 6. Elongation of the CL along the AL.

Fig. 7. Full restoration of intestinal continuity.

cholesterol metabolism (Fig. 8).

We prefer to section the alimentary limb (AL) immediately proximal to the enteroenterostomy (EEA) and join the ileal stump to the jejunum, immediately distal to the ligament of Treitz. This type of restoration allows the resumption of a normal proteinenergy absorption, still partially preserving both the specific effects of BPD on glucose and

Fig. 8. Restoration bringing the AL to the ligament of Treitz.

Fig. 9. Restoration bringing the AL to the duodenum.

Restoration may be necessary if **a disease occurs whose consequences would be worsened by malabsorption**, e.g., liver cirrhosis, nephrotic syndrome, chronic inflammatory bowel disease, malignancy, or psychosis. It may also be requested by the BPD subject instead of the elongation after a long period of recurrent PM, or for different reasons, e.g., intolerance of the stool/gas problems, or psychological intolerance of the environmental problems

BPD and BPD-DS Concerns and Results 201

adaptation), as shown in Figure 9. The patient slowly lost all the excessive weight previously regained. The same operation was subsequently successfully used in another case that had been submitted to BPD elsewhere and had had minimal weight reduction. Both the CL and the AL were excessively long, and this most probably was due to wrong intestinal measurement, even if a rapidly occurring excessive intestinal adaptation could not

The total number of revisions in the last consecutive 1000 AHS-AHAL BPD patients with a minimum follow-up of 1 year was 10 or 1.0%, 4 (0.4%) being elongation of the CL and 6 (0.6%) restorations of intestinal continuity. The latter cases presented with ensuing medical problems, unrelated to the operation, which necessitated resumption of normal protein

All problems of recurrent PM, excessive weight loss, diarrhea, stool/gas, and bone demineralization permanently disappeared after revisions. While no recurrences of hypercholesterolemia were ever observed, there were two cases of mild hyperglycemia in

Since protein and starch digestion/absorption occur in the entire small bowel between the GEA and the ICV, and fat absorption in the intestinal segment between the EEA and the ICV, the elongation of the CL along the BPL which is necessary to increase protein absorption also causes an increase of starch and fat absorption. This obviously results in a higher energy absorption threshold, which explains the restabilization at a higher body weight of the subjects undergoing elongation of the CL for recurrent PM and/or excessive

The subjects who were elongated along the AL because of diarrhea from excessive bile salt malabsorption had and maintained a food intake equal to the preoperative one, and they

The weight changes after BPD revisions indicate that, when the indication was correctly given by us according to the physiology of the operation, the revised subjects had a moderate weight regain with restabilization, the success being maintained, while in the

A final consideration regards the mean weight loss at the time of revision, which was in most cases lower than the average in our series. Any degree of weight reduction can be obtained with BPD, but, as we learned at our expenses, the greater the mean weight loss, the greater the number of problems. Unless a surgeon has an experience sufficient to enable him to tailor the operation on each single subject, any mean reduction of the IEW greater than 70% should be considered potentially dangerous. Weight maintenance, not weight loss, is

did not gain any weight in a 6- and 11-year follow-up, respectively.

other cases they regained weight progressively toward failure.

be ruled out.

**8.5 Timing**

absorption

**8.6 Secondary effects**

**8.7 Weight regain**

weight loss.

the real magic of BPD.

previously diabetic patients after elongation.

originated by the changed body shape, or what we simply call **"intolerance of the operation."**

Only in case of **intractable severe bone demineralization**, or of moderate bone demineralization associated with a condition that indicates the restoration, we accept the sacrifice of the effect on glucose metabolism by putting the duodenum in the alimentary continuity, which can be accomplished as shown in Figure 34–3, or, if the effect on cholesterol metabolism is to be preserved, by keeping the entire AL interposed between the stomach and the duodenum (Fig. 9).

Fig. 10. Shorting of both alimentary and the common.

Exceptionally, a shortening of the intestinal limbs may be considered. The most common cause for **weight regain** after BPD is excessive intake of simple sugar. Only if this type of **patient's noncompliance** can be reasonably excluded, an excess of the adaptive phenomena leading to late energy absorption increase may be suspected. A preliminary measurement of alimentary protein intestinal absorption is, in our opinion, mandatory. More than 90% absorption on the one hand confirms the excessive adaptation, on the other hand it means that there is a wide margin for shortening without causing excessive protein malabsorption.

In two cases, both with 370-cm AL, we resected the proximal part of the AL exceeding the 240cm which, as a mean of the intestinal measurements taken at late reoperations for any cause, result after adaptation, with redo of GEA. Since these two patients failed to lose weight, we thought it could be due to the highly consuming small bowel removed, which compensated for the decreased absorption. In a third case, with 520-cm AL and 80-cm CL, we sectioned the AL 240 cm distal to the GEA, detached the biliopancreatic limb (BPL) from the distal ileum, and then anastomosed the BPL to the distal stump of the AL section and the proximal stump to the distal ileum, thus creating a CL of 70 cm (mean CL length after adaptation), as shown in Figure 9. The patient slowly lost all the excessive weight previously regained. The same operation was subsequently successfully used in another case that had been submitted to BPD elsewhere and had had minimal weight reduction. Both the CL and the AL were excessively long, and this most probably was due to wrong intestinal measurement, even if a rapidly occurring excessive intestinal adaptation could not be ruled out.

#### **8.5 Timing**

200 Advanced Bariatric and Metabolic Surgery

originated by the changed body shape, or what we simply call **"intolerance of the**

Only in case of **intractable severe bone demineralization**, or of moderate bone demineralization associated with a condition that indicates the restoration, we accept the sacrifice of the effect on glucose metabolism by putting the duodenum in the alimentary continuity, which can be accomplished as shown in Figure 34–3, or, if the effect on cholesterol metabolism is to be preserved, by keeping the entire AL interposed between the

Exceptionally, a shortening of the intestinal limbs may be considered. The most common cause for **weight regain** after BPD is excessive intake of simple sugar. Only if this type of **patient's noncompliance** can be reasonably excluded, an excess of the adaptive phenomena leading to late energy absorption increase may be suspected. A preliminary measurement of alimentary protein intestinal absorption is, in our opinion, mandatory. More than 90% absorption on the one hand confirms the excessive adaptation, on the other hand it means that there is a wide margin for shortening without causing excessive

In two cases, both with 370-cm AL, we resected the proximal part of the AL exceeding the 240cm which, as a mean of the intestinal measurements taken at late reoperations for any cause, result after adaptation, with redo of GEA. Since these two patients failed to lose weight, we thought it could be due to the highly consuming small bowel removed, which compensated for the decreased absorption. In a third case, with 520-cm AL and 80-cm CL, we sectioned the AL 240 cm distal to the GEA, detached the biliopancreatic limb (BPL) from the distal ileum, and then anastomosed the BPL to the distal stump of the AL section and the proximal stump to the distal ileum, thus creating a CL of 70 cm (mean CL length after

**operation."**

stomach and the duodenum (Fig. 9).

Fig. 10. Shorting of both alimentary and the common.

protein malabsorption.

The total number of revisions in the last consecutive 1000 AHS-AHAL BPD patients with a minimum follow-up of 1 year was 10 or 1.0%, 4 (0.4%) being elongation of the CL and 6 (0.6%) restorations of intestinal continuity. The latter cases presented with ensuing medical problems, unrelated to the operation, which necessitated resumption of normal protein absorption

#### **8.6 Secondary effects**

All problems of recurrent PM, excessive weight loss, diarrhea, stool/gas, and bone demineralization permanently disappeared after revisions. While no recurrences of hypercholesterolemia were ever observed, there were two cases of mild hyperglycemia in previously diabetic patients after elongation.

#### **8.7 Weight regain**

Since protein and starch digestion/absorption occur in the entire small bowel between the GEA and the ICV, and fat absorption in the intestinal segment between the EEA and the ICV, the elongation of the CL along the BPL which is necessary to increase protein absorption also causes an increase of starch and fat absorption. This obviously results in a higher energy absorption threshold, which explains the restabilization at a higher body weight of the subjects undergoing elongation of the CL for recurrent PM and/or excessive weight loss.

The subjects who were elongated along the AL because of diarrhea from excessive bile salt malabsorption had and maintained a food intake equal to the preoperative one, and they did not gain any weight in a 6- and 11-year follow-up, respectively.

The weight changes after BPD revisions indicate that, when the indication was correctly given by us according to the physiology of the operation, the revised subjects had a moderate weight regain with restabilization, the success being maintained, while in the other cases they regained weight progressively toward failure.

A final consideration regards the mean weight loss at the time of revision, which was in most cases lower than the average in our series. Any degree of weight reduction can be obtained with BPD, but, as we learned at our expenses, the greater the mean weight loss, the greater the number of problems. Unless a surgeon has an experience sufficient to enable him to tailor the operation on each single subject, any mean reduction of the IEW greater than 70% should be considered potentially dangerous. Weight maintenance, not weight loss, is the real magic of BPD.

BPD and BPD-DS Concerns and Results 203

Imaging and endoscopic studies are necessary to study the problem and give an accurate map of the existing anatomy. As restrictive bariatric procedures are practiced following different techniques with modifications of some of the originally described steps, it is advisable to read the operative note or to discuss the case with the surgeon who carried out

Revisional bariatric surgery is technically demanding. There are technical aspects common to any reoperation after gastric surgeries that need to be taken into account to minimize

Adhesions are likely to be present and they may be anywhere. Therefore, access to the cavity should be attained by open technique, or alternatively using an optical trocar, trying

Once in the cavity, following ports should be placed in an order that allows dividing the adhesions from the best point of view. In addition, liver retraction should be done delicately, and only after its adhesions have been addressed, because any sudden movement or excessive force could produce a tear, and bleeding will obscure the surgical field,

Division of gastric vessels should only be carried out after the gastric vascular supply has been assessed. Restrictive procedures usually preserve lesser curvature vessels, and therefore these should be preserved at all costs. If the left gastric artery or its branches need to be cut at some stage, the condition of the stomach must to be carefully observed to rule

Intraoperative endoscopy is a valuable tool when during the procedure it is difficult to accurately characterize the anatomic changes seen during the laparoscopy. It should be

Laparoscopic surgery has had a major impact on obesity surgery the last decade. All bariatric procedures have been proven to be technically feasible via laparoscopy (Buchwald et al, 2004). There is also evidence that the laparoscopic approach is advantageous, since it is associated with less perioperative morbidity and faster recovery (The Society of American Gastrointestinal and Endoscopic Surgeons (SAGES) Guidelines Committee , 2008; Weller

scheduled beforehand to avoid delays in a possibly long intervention.

1. History and Physical examination;

Symptoms of acid hypersecretion Screening for eating disorders Psychological evaluation if positive

3. Barium swallow to document anatomy 4. EGD if patient has symptoms of GERD

2. Review old operative notes and videos if possible

Symptoms of dysmotility

BMI

the index surgery.

complications.

**9.4 General considerations**

to prevent visceral injuries.

reducing visibility and causing delays.

out ischemia leading to gastric resection.

**9.5 Open versus laparoscopic approach**

### **9. Revision to BPD**

The superior results of BPD both in weight maintenance and control of component of metabolic syndrome make this operation a good choice for revision of failed other types of bariatric procedures. Furthermore, revision to BPD often enables the surgeon to avoid scarred tissue high up in the stomach, thus simplifying reoperation and reducing perioperative morbidity.

Revisional Bariatric surgery is technically challenging and becoming more common due to the rapid increase in patients undergoing surgery for morbid obesity. Unfortunately, there is no sufficient evidence to help the surgeon deciding which revisional procedure to choose based. There are several factors that need to be considered when unsatisfactory outcomes after bariatric surgery are obtained.

The extent of weight loss may not be the only factor to be considered while evaluating the results of a bariatric restrictive procedure, because the major goal of bariatric procedures is the cure or control of comorbidities along with the weight loss. With this idea in mind, a borderline weight loss with a successful control of comorbidities (eg, easier hypertension or diabetes control, disappearance of articular pain or swelling, cure of sleep apnea, etc.) in a high-risk patient without surgery-related complications should probably be considered a good outcome, and the patient could avoid additional surgery. These issues should be clarified with the patient when discussing risks and benefits of the reoperation.

Both patient and surgeon need to be aware that a new operation will be a difficult task, and realistic goals have to be presented to the patient. There is a higher risk of complications, and a possibility that a new bariatric procedure may not be completed in one intervention as planned owing to inflammation, scarring, and bleeding. Patients must know that more than one intervention may be required. Unlike gastric restrictive revisional surgery, revision to BPD usually does not impair final weight loss results.

#### **9.1 Indications for revision**

#### **9.2 Patient evaluation**

Surgeons should consider that failure of specific restrictive bariatric procedures is owing to many factors. One of these factors is patient's compliance with the dietary program, and when required, with behavioral modifications after the primary procedure. Patients may not need a second surgery but a close follow-up and behavior counseling before deciding on a more drastic intervention.

#### **9.3 Approach to the patient**

Detailed evaluation of the preoperative data of the these patients, operative notes and postoperative BMI and complications through a Pre-operative check-list;

The superior results of BPD both in weight maintenance and control of component of metabolic syndrome make this operation a good choice for revision of failed other types of bariatric procedures. Furthermore, revision to BPD often enables the surgeon to avoid scarred tissue high up in the stomach, thus simplifying reoperation and reducing

Revisional Bariatric surgery is technically challenging and becoming more common due to the rapid increase in patients undergoing surgery for morbid obesity. Unfortunately, there is no sufficient evidence to help the surgeon deciding which revisional procedure to choose based. There are several factors that need to be considered when unsatisfactory outcomes

The extent of weight loss may not be the only factor to be considered while evaluating the results of a bariatric restrictive procedure, because the major goal of bariatric procedures is the cure or control of comorbidities along with the weight loss. With this idea in mind, a borderline weight loss with a successful control of comorbidities (eg, easier hypertension or diabetes control, disappearance of articular pain or swelling, cure of sleep apnea, etc.) in a high-risk patient without surgery-related complications should probably be considered a good outcome, and the patient could avoid additional surgery. These issues should be

Both patient and surgeon need to be aware that a new operation will be a difficult task, and realistic goals have to be presented to the patient. There is a higher risk of complications, and a possibility that a new bariatric procedure may not be completed in one intervention as planned owing to inflammation, scarring, and bleeding. Patients must know that more than one intervention may be required. Unlike gastric restrictive revisional surgery, revision to

Surgeons should consider that failure of specific restrictive bariatric procedures is owing to many factors. One of these factors is patient's compliance with the dietary program, and when required, with behavioral modifications after the primary procedure. Patients may not need a second surgery but a close follow-up and behavior counseling before deciding on a

Detailed evaluation of the preoperative data of the these patients, operative notes and

postoperative BMI and complications through a Pre-operative check-list;

clarified with the patient when discussing risks and benefits of the reoperation.

BPD usually does not impair final weight loss results.

3. Complications of previous the procedure.

**9. Revision to BPD**

perioperative morbidity.

after bariatric surgery are obtained.

**9.1 Indications for revision**  1. Insufficient weight loss.

2. Weight regain.

**9.2 Patient evaluation**

more drastic intervention.

**9.3 Approach to the patient**

1. History and Physical examination; BMI

Symptoms of dysmotility Symptoms of acid hypersecretion Screening for eating disorders Psychological evaluation if positive

Imaging and endoscopic studies are necessary to study the problem and give an accurate map of the existing anatomy. As restrictive bariatric procedures are practiced following different techniques with modifications of some of the originally described steps, it is advisable to read the operative note or to discuss the case with the surgeon who carried out the index surgery.

#### **9.4 General considerations**

Revisional bariatric surgery is technically demanding. There are technical aspects common to any reoperation after gastric surgeries that need to be taken into account to minimize complications.

Adhesions are likely to be present and they may be anywhere. Therefore, access to the cavity should be attained by open technique, or alternatively using an optical trocar, trying to prevent visceral injuries.

Once in the cavity, following ports should be placed in an order that allows dividing the adhesions from the best point of view. In addition, liver retraction should be done delicately, and only after its adhesions have been addressed, because any sudden movement or excessive force could produce a tear, and bleeding will obscure the surgical field, reducing visibility and causing delays.

Division of gastric vessels should only be carried out after the gastric vascular supply has been assessed. Restrictive procedures usually preserve lesser curvature vessels, and therefore these should be preserved at all costs. If the left gastric artery or its branches need to be cut at some stage, the condition of the stomach must to be carefully observed to rule out ischemia leading to gastric resection.

Intraoperative endoscopy is a valuable tool when during the procedure it is difficult to accurately characterize the anatomic changes seen during the laparoscopy. It should be scheduled beforehand to avoid delays in a possibly long intervention.

#### **9.5 Open versus laparoscopic approach**

Laparoscopic surgery has had a major impact on obesity surgery the last decade. All bariatric procedures have been proven to be technically feasible via laparoscopy (Buchwald et al, 2004). There is also evidence that the laparoscopic approach is advantageous, since it is associated with less perioperative morbidity and faster recovery (The Society of American Gastrointestinal and Endoscopic Surgeons (SAGES) Guidelines Committee , 2008; Weller

BPD and BPD-DS Concerns and Results 205

significantly reduce the incidence of anastomotic ulcers. By transferring these observations to bariatric context, the goal of the Duodenal Switch (DS) variation of Biliopancreatic Diversion (BPD) proposed by Douglas Hess and Picard Marceau was to reduce the complications correlated with Scopinaro's original procedure while maintaining its long-

The modifications adopted in DS are: modifying the distal gastrectomy of the BPD with a vertical gastrectomy along the greater curvature (sleeve gastrectomy). Further modification foresaw the lengthening of the common channel to 100cm, thus doubling the length of the absorbent common ileal segment, for greater control of the number of daily bowel movements. Some procedures that are consensual to BPD, like cholecystectomy, appendectomy and liver biopsies were routinely performed by different authors even in the DS variation. These modifications have led, according to the same authors, to the reduction in the incidence of dumping syndrome, anastomotic ulcer, and proteins malabsorption.

Analysing the results of open BPD vs. DS, Marceau reports fewer daily evacuations, less diarrhea, vomiting and bone pain following DS associated with higher serum levels of

Whether this report is simply the result of a progressive learning curve (standard BPD had been adopted in the early experience, and BPD with DS had been further developed in later years), or if the longer length of the common channel, by increasing bile acid absorption, and thus lowering the degree of steatorrhea, leads to fewer bowel movements per day, and, consequently, to less endogenous nitrogen loss, has never been studied in a prospective fashion. In fact, most recent publications report very similar results and side effects for both operations. Just as for standard BPD, BPD- DS primarily induces malabsorption of fats due to the diversion of bile and pancreatic enzymes to the common limb. Therefore, the length of the alimentary limb and the common limb is of the fundamental importance; if the common channel is too long, the malabsorption of fats might not be sufficient to guarantee an adequate weight loss over the long term; an excessively long alimentary limb leads to

Duodenal switch might nonetheless be a better option in revision of failed sleeve gastrectomies, as the latter operation had in fact been introduced in clinical practice as the

Suture line dehiscence can occur at the gastric suture after sleeve gastrectomy, at both anastomoses and at the duodenal stump. The incidence of suture-line leak after sleeve gastrectomy ranges between 1.3% and 4.6% (Hess, 1998, Lee et al, 2007). The critical areas for leak are the top of the suture line and the transition point between sequential cartridges. To prevent leak many authors suggest reinforcing the long suture line with buttress material, a running suture or fibrin glue. The suture line fistula can be managed by percutaneous

term effectiveness on weight loss and co-morbidities resolution.

insufficient weight loss for insufficient malabsorption of starch.

first stage of BPD-DS in super-superobese patients.

**10.2 Peri- and postoperative complications**

**10.2.1 Fistula**

**10.1 Modifications**

ferritin, calcium and Vitamin A.

Rosati, 2008) . Laparoscopic approach to malabsorption procedures, such as the BPD or the duodenal switch operation (DS), is more complex and technically difficult (Scopinaro et al, 2002; Baltasar et al, 2002; Weiner et al, 2004). Several reports have demonstrated the efficacy of laparoscopic revisional bariatric surgery (Gumbs et al, 2007). However, laparoscopic redo surgery, after failed primary bariatric procedures, should be handled cautiously. Van Dessel et al, 2008 reported recently that the threshold for conversion to open approach should be low.

In patients after failed or complicated bariatric operations, it is the surgical management that eventually matters and not the approach.

#### **9.6 Which type of revision? And why BPD?**

Surgeons differ in their management of failed bariatric procedures, depending on their individual experience and resultant choice of surgical operation or operations. Revision of failed gastric restrictive operation is a common problem today, and is likely to increase in the near future (Sarr, 2007). In our opinion, the conversion of a restrictive operation to a malabsorptive one appears for some patients as the only alternative to cope with poor weight loss results. Such conversions, after unsuccessful weight loss, have been previously described (Fox, 1991; Keshishian et al, 2004; Di Betta et al, 2006). Since gastric bypass relies primarily on restriction, a different surgical approach, based essentially on malabsorption was employed as the final option in this cohort of patients with multiple previous bariatric interventions. In a recent report, (Topart et al, 2007) demonstrated that BPD with duodenal switch resulted in greater weight loss compared to Roux-en-Y gastric bypass after failed gastric banding. However, BPD-DS resulted in a higher early complication rate. When compared to RYGB, BPD and BPD-DS procedures are suggested to create superior weight loss and more accurately, superior weight loss maintenance (DeMaria, 2004).

In a recent analysis, it was demonstrated that obesity surgery results depend on the performed technique. BPD was proven to be the only operation that kept excellent weight results in time but unfortunately, with increased morbidity (Gracia et al, 2009). So far, no adequate prospective trial has been done to adequately answer the question of "which revisional bariatric procedure to do" in the setting of inadequate weight loss or excessive weight regain (Gumbs et al, 2007).

Furthermore, failed RYGB represent a subset of particularly challenging cases, in which only BPD can provide adequate results. Conversion from RYGB to biliopancreatic diversion with duodenal switch (BPD-DS) might provide the most durable weight loss of all revision procedures currently available. Revision to BPD-DS can be done laparoscopically in 1 or 2 stages and involves 4 anastomoses: gastrogastrostomy, duodenoileostomy, ileoileostomy, and jejunojejunostomy (to reconnect the old Roux limb).

#### **10. Duodenal switch**

Duodenal Switch (DS), is the malabsorptive procedure that is usually performed in North America for treatment of morbid obesity. In 1987, DeMeester, in some experimental studies conducted on biliary gastritis, showed that keeping even a short duodenal limb could significantly reduce the incidence of anastomotic ulcers. By transferring these observations to bariatric context, the goal of the Duodenal Switch (DS) variation of Biliopancreatic Diversion (BPD) proposed by Douglas Hess and Picard Marceau was to reduce the complications correlated with Scopinaro's original procedure while maintaining its longterm effectiveness on weight loss and co-morbidities resolution.

#### **10.1 Modifications**

204 Advanced Bariatric and Metabolic Surgery

Rosati, 2008) . Laparoscopic approach to malabsorption procedures, such as the BPD or the duodenal switch operation (DS), is more complex and technically difficult (Scopinaro et al, 2002; Baltasar et al, 2002; Weiner et al, 2004). Several reports have demonstrated the efficacy of laparoscopic revisional bariatric surgery (Gumbs et al, 2007). However, laparoscopic redo surgery, after failed primary bariatric procedures, should be handled cautiously. Van Dessel et al, 2008 reported recently that the threshold for conversion to open approach

In patients after failed or complicated bariatric operations, it is the surgical management

Surgeons differ in their management of failed bariatric procedures, depending on their individual experience and resultant choice of surgical operation or operations. Revision of failed gastric restrictive operation is a common problem today, and is likely to increase in the near future (Sarr, 2007). In our opinion, the conversion of a restrictive operation to a malabsorptive one appears for some patients as the only alternative to cope with poor weight loss results. Such conversions, after unsuccessful weight loss, have been previously described (Fox, 1991; Keshishian et al, 2004; Di Betta et al, 2006). Since gastric bypass relies primarily on restriction, a different surgical approach, based essentially on malabsorption was employed as the final option in this cohort of patients with multiple previous bariatric interventions. In a recent report, (Topart et al, 2007) demonstrated that BPD with duodenal switch resulted in greater weight loss compared to Roux-en-Y gastric bypass after failed gastric banding. However, BPD-DS resulted in a higher early complication rate. When compared to RYGB, BPD and BPD-DS procedures are suggested to create superior weight

In a recent analysis, it was demonstrated that obesity surgery results depend on the performed technique. BPD was proven to be the only operation that kept excellent weight results in time but unfortunately, with increased morbidity (Gracia et al, 2009). So far, no adequate prospective trial has been done to adequately answer the question of "which revisional bariatric procedure to do" in the setting of inadequate weight loss or excessive

Furthermore, failed RYGB represent a subset of particularly challenging cases, in which only BPD can provide adequate results. Conversion from RYGB to biliopancreatic diversion with duodenal switch (BPD-DS) might provide the most durable weight loss of all revision procedures currently available. Revision to BPD-DS can be done laparoscopically in 1 or 2 stages and involves 4 anastomoses: gastrogastrostomy, duodenoileostomy, ileoileostomy,

Duodenal Switch (DS), is the malabsorptive procedure that is usually performed in North America for treatment of morbid obesity. In 1987, DeMeester, in some experimental studies conducted on biliary gastritis, showed that keeping even a short duodenal limb could

loss and more accurately, superior weight loss maintenance (DeMaria, 2004).

should be low.

that eventually matters and not the approach.

**9.6 Which type of revision? And why BPD?**

weight regain (Gumbs et al, 2007).

**10. Duodenal switch**

and jejunojejunostomy (to reconnect the old Roux limb).

The modifications adopted in DS are: modifying the distal gastrectomy of the BPD with a vertical gastrectomy along the greater curvature (sleeve gastrectomy). Further modification foresaw the lengthening of the common channel to 100cm, thus doubling the length of the absorbent common ileal segment, for greater control of the number of daily bowel movements. Some procedures that are consensual to BPD, like cholecystectomy, appendectomy and liver biopsies were routinely performed by different authors even in the DS variation. These modifications have led, according to the same authors, to the reduction in the incidence of dumping syndrome, anastomotic ulcer, and proteins malabsorption.

Analysing the results of open BPD vs. DS, Marceau reports fewer daily evacuations, less diarrhea, vomiting and bone pain following DS associated with higher serum levels of ferritin, calcium and Vitamin A.

Whether this report is simply the result of a progressive learning curve (standard BPD had been adopted in the early experience, and BPD with DS had been further developed in later years), or if the longer length of the common channel, by increasing bile acid absorption, and thus lowering the degree of steatorrhea, leads to fewer bowel movements per day, and, consequently, to less endogenous nitrogen loss, has never been studied in a prospective fashion. In fact, most recent publications report very similar results and side effects for both operations. Just as for standard BPD, BPD- DS primarily induces malabsorption of fats due to the diversion of bile and pancreatic enzymes to the common limb. Therefore, the length of the alimentary limb and the common limb is of the fundamental importance; if the common channel is too long, the malabsorption of fats might not be sufficient to guarantee an adequate weight loss over the long term; an excessively long alimentary limb leads to insufficient weight loss for insufficient malabsorption of starch.

Duodenal switch might nonetheless be a better option in revision of failed sleeve gastrectomies, as the latter operation had in fact been introduced in clinical practice as the first stage of BPD-DS in super-superobese patients.

#### **10.2 Peri- and postoperative complications**

#### **10.2.1 Fistula**

Suture line dehiscence can occur at the gastric suture after sleeve gastrectomy, at both anastomoses and at the duodenal stump. The incidence of suture-line leak after sleeve gastrectomy ranges between 1.3% and 4.6% (Hess, 1998, Lee et al, 2007). The critical areas for leak are the top of the suture line and the transition point between sequential cartridges. To prevent leak many authors suggest reinforcing the long suture line with buttress material, a running suture or fibrin glue. The suture line fistula can be managed by percutaneous

BPD and BPD-DS Concerns and Results 207

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Borg CM, le Roux CW, Ghatei MA, et al. (2007) Biliopancreatic Diversion in Rats is

Brandi LS, Santoro D, Natali A, et al. (1993) Insulin Resistance of Stress: Sites and

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Buchwald H, Estok R, Fahrbach K, et al. (2009) Weight and Type 2 Diabetes after Bariatric Surgery: Systematic Review and Meta analysis. Am J Med.122, 248–256. Civalleri D, Scopinaro G, Gianetta E, et al. (1982)Assorbimento della vitamina B12 dopo bypass biliopancreatico per l'obesit`a. Min Diet Gastroenterol. 28, 181–188. Civalleri D, Gianetta E, FriedmanD, et al. (1986): Changes of gastric acid secretion after

Compston JE,Vedi S, Gianetta E, et al. (1984) Bone histomorphometry and vitamin D status after biliopancreatic bypass for obesity. Gastroenterology, 87, 350–356. Crowley LV, Seay J, Mullin GT Jr, et al. (1986). Long term hematopoietic and skeletal effects

DeMaria EJ. (2004) Is gastric bypass superior for the surgical treatment of obesity compared

Di Betta E, Mittempergher F, Di Fabio F, et al. (2006) Duodenal switch without gastric

Doyle ME, Egan JM. (2007). Mechanisms of Action of Glucagone-like Peptide 1 in the

Farilla L, Bulotta A, Hirshberg B, et al. (2003) Glucagon-like Peptide 1 Inhibits Cell

Fisher AB: (1984). Twenty-five years after Billroth II gastrectomy for duodenal ulcer.World J

Forbes GB. (1987). Human Body composition; Growth, aging and nutrition and activity.

Fox SR. (1991) The use of biliopancreatic diversion as a treatment for failed gastric

Gianetta E, Civalleri D, Bonalumi U, et al. (1980). Studio dell'assorbimento proteico dopo bypass bilio-pancreatico per l'obesit`a. MinDiet e Gastr, 26, 251–256. Gianetta E, Civalleri D, Bonalumi U, et al. (1981). Studio dell'assorbimento lipidico dopo

Gianetta E, Friedman D, Adami GF, et al. (1985). Effects of biliopancreatic bypass on

hypercholesterolemia and hypertriglyceridemia. In: Proceedings of the Second Annual Meeting of the American Society forBariatric Surgery, Iowa City, IA, June

bypass biliopancreatico per l'obesit`a. Min Diet e Gastr, 27, 65–70.

resection after failed gastric restrictive surgery for morbid obesity. Obes Surg, 16,

Apoptosis and Improve Glucose Responsiveness of Freshly Isolated Human Islets.

partial biliopancreatic bypass. Clin Nutr, 5 (Suppl), 215– 220.

with malabsorptive procedures? J Gastrointest Surg, 8, 401–403.

Eddy RL: (1984) Metabolic bone disease after gastrectomy. AmJMed, 8, 293–302.

partitioning in the morbidly obese. Obes Surg, 1, 89–93.

of gastric bypass. Clin Nutr, 5(Suppl),185–187.

Pancreas. Pharmacol Ther,113, 546–593.

Endocrinology,144, 5149– 5158.

Springer Verlag New York, 1987.

258–261.

Surg 8:293–302,.

1985.

triglycerides. Metabolism.31, 438–444.

Mechanisms. Clin Sci (Lond).85, 525–535.

meta-analysis. JAMA. 292, 1724– 1737.

levels. Obes Surg.17, 1193–1198.

circulation of bile acids on the transport of very low density-lipoprotein

Associated with Intestinal Hypertrophy and with Increased GLP-1, GLP-2 and PYY

drainage plus total parenteral nutrition and antibiotics associated, in selected cases, with endoscopic stenting.

Anastomotic leak seems to have the same incidence rate in LapBPD-DS as in the open series (2.5%) (Marceau et al, 1998, Ren et al, 2000, Lee et al, 2007). The clinical presentations involves tachycardia (heart rate >120 beats /minute), fever, abdominal pain, hypotension and mental deadness. To make the correct diagnosis an upper GI X-ray can be useful, but a negative contrast X-ray study does not exclude a fistula.

Therefore, a spiral angioCT scan is the most accurate diagnostic tool in doubtful cases. In case of low output fitulas and when there are no signs of haemodynamic instability, management could be conservative. Failure of nonoperative management or signs of peritonitis, a laparoscopic or laparoscopic reoperation is indicated. Options includes suture of the anastomotic dehiscence, wide drainage and/or with the creation of a jejunostomy in the biliopancreatic limb for decompression and for enteral nutrition and supportive care. Compared to the most recent series of standard BPD, fistula incidence after BPD-DS seems higher.

#### **11. Conclusions**

BPD yields the best results obtained in the treatment of obesity and metabolic syndrome. The reasons why, although in use for more than 35 years, this operation still has relatively minimal diffusion in the world are many, and they have little to do with its effectiveness and safety. However, this is to be considered a favorable event: BPD would cause dramatic damages if improperly used, and this would certainly happen if the operation had a rapid diffusion among the average bariatric surgeon. For the same reason, being able to master BPD and its complications, and understanding its pathophysiology, is extremely important for a committed bariatric surgeon, because, *at the very least*, it represents a very powerful and effective weapon in difficult revisional cases and in the metabolically highly compromised patient. To be limited to a slowly increasing number of good hands is the main guarantee of safety for biliopancreatic diversion.

#### **12. References**

drainage plus total parenteral nutrition and antibiotics associated, in selected cases, with

Anastomotic leak seems to have the same incidence rate in LapBPD-DS as in the open series (2.5%) (Marceau et al, 1998, Ren et al, 2000, Lee et al, 2007). The clinical presentations involves tachycardia (heart rate >120 beats /minute), fever, abdominal pain, hypotension and mental deadness. To make the correct diagnosis an upper GI X-ray can be useful, but a

Therefore, a spiral angioCT scan is the most accurate diagnostic tool in doubtful cases. In case of low output fitulas and when there are no signs of haemodynamic instability, management could be conservative. Failure of nonoperative management or signs of peritonitis, a laparoscopic or laparoscopic reoperation is indicated. Options includes suture of the anastomotic dehiscence, wide drainage and/or with the creation of a jejunostomy in the biliopancreatic limb for decompression and for enteral nutrition and supportive care. Compared to the most recent series of standard BPD, fistula incidence after BPD-DS seems

BPD yields the best results obtained in the treatment of obesity and metabolic syndrome. The reasons why, although in use for more than 35 years, this operation still has relatively minimal diffusion in the world are many, and they have little to do with its effectiveness and safety. However, this is to be considered a favorable event: BPD would cause dramatic damages if improperly used, and this would certainly happen if the operation had a rapid diffusion among the average bariatric surgeon. For the same reason, being able to master BPD and its complications, and understanding its pathophysiology, is extremely important for a committed bariatric surgeon, because, *at the very least*, it represents a very powerful and effective weapon in difficult revisional cases and in the metabolically highly compromised patient. To be limited to a slowly increasing number of good hands is the main guarantee of

Adami GF, Compston JE, Gianetta E, et al.(1987) Changes in bone histomorphometry

Adami GF, Gandolfo P, Esposito M, et al. (1991). Orally-administered serum ranitidine concentration after biliopancreatic diversion. Obes Surg, 1, 293–294. Adami GF, Cordera R, Camerini G, et al. (2003) Recovery of Insulin Sensitivity in Obese Patients at Short Term after Biliopancreatic Diversion.J Surg Res.113, 217–221. Adami GF, Murelli F, Briatore L, et al. (2008). Pregnancy in Formerly Type 2 Diabetes

Baltasar A, Bou R, Miró J, et al. (2002)Laparoscopic biliopancreatic diversion with duodenal

Ast M, Frishman WH. (1990) Bile acid sequestrants. J Clin Pharmacol.30, 99–106.

switch: technique and initial experience. Obes Surg.12, 245–248.

*on Obesity Surgery,* Genoa, Italy, September 1987.

following biliopancreatic diversion. In: *Proceedings of the III International Symposium*

Obese Women Following Biliopancreatic Diversion for Obesity. Obes Surg.18,

negative contrast X-ray study does not exclude a fistula.

endoscopic stenting.

higher.

**11. Conclusions**

**12. References**

safety for biliopancreatic diversion.

1109–1111.

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Scopinaro N, Gianetta E, Civalleri D, et al. (1979) . Bilio-pancreatic by-pass for obesity, II:

Scopinaro N, Gianetta E, Civalleri D, et al. (1980) . Two years of clinical experience with

ScopinaroN, Gianetta E, FriedmanD, et al. (1992) . Biliopancreatic diversion for obesity.

Scopinaro N, Gianetta E, Adami GF, et al. (1996) . Biliopancreatic diversion for obesity at

Scopinaro N, Adami GF, Marinari G, et al. (1997) . The effect of biliopancreatic diversion on

Scopinaro N, Marinari GM, Gianetta E, et al. (1997) . The respective importance of the

Scopinaro N, Adami GF, Marinari GM, et al. (1998) . Biliopancreatic diversion. World J

Scopinaro N, Marinari GM, Adami GF, et al. (1999) . The influence of gastric volume on

Scopinaro N, Marinari GM, Camerini G, et al. (2000) . Energy and nitrogen absorption after

Scopinaro N, Marinari GM, Camerini G. (2002) . Laparoscopic standard biliopancreatic diversion: technique and preliminary results. Obes Surg , 12 , 241–244. Scopinaro N, Marinari GM, Camerini GB, et al. (2005) . Specific Effects of Biliopancreatic

Scopinaro N, Papadia F, Camerini G, et al. (2008) . A Comparison of a Personal Series of

Scopinaro N, Adami GF, Papadia FS, et al. (2011) . Effects of biliopancreatic diversion on type 2 diabetes in patients with BMI 25–35. Ann Surg , 253 , 699–703. Storer EH,Woodward ER, Dragstedt LR: (1950) . The effect of vagotomy and antrum

Thorell A, Nygren J, Ljungqvist O. (1999) Insulin Resistance: A Marker of Surgical Stress.

Topart P, Becouarn G, Ritz P. (2007) . Biliopancreatic diversion with duodenal switch or

Valverde I, Puente J,Martín-Duce A, et al. (2005) Changes in Glucagon-like Peptide-1 (GLP-

Van Dessel E, Hubens G, Ruppert M, et al. (2008). Roux-en-Y gastric bypass as a re-do procedure for failed restricive gastric surgery. Surg Endosc , 22 , 1014–1018. Weiner RA, Blanco-Engert R, Weiner S, et al. (2004) . Laparoscopic biliopancreatic diversion

Weller WE, Rosati C. (2008) . Comparing outcomes of laparoscopic versus open bariatric

gastric bypass for failed gastric banding: retrospective study from two institutions

1) Secretion after Biliopancreatic Diversion or Vertical Banded Gastroplasty in

with duodenal switch: three different duodeno-ileal anastomotic techniques and

resection on the Mann-Williamson ulcer. Surgery , 27 , 526– 530.

with preliminary results. Surg Obes Relat Dis , 3 , 521–525.

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Biliopancreatic Diversion and Literature Data on Gastric Bypass Help to Explain the Mechanisms of Resolution of Type 2 Diabetes by the Two Operations. Obes

energy and protein absorption after BPD. Obes Surg , 2 , 125–126.

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biliopancreatic bypass for obesity. Amer J Clin Nutr, 33 , 506–514.

Initial experience in man. Br J Surg , 66 , 619–620.

Probl Gen Surg , 9 , 362–379.

BPD. Obes Surg, 7 , 108.

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Surg ,18 ,1035–1038.

eighteen years. Surgery, 119 , 261–268.

glucose metabolism. Obes Surg, 7 , 296–297.

biliopancreatic diversion. Obes Surg , 10 , 436–441.

up Study. Diabetes Care , 28 , 2406–2411.

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Obese Subjects. Obes Surg ,15 , 387–397.

initial experience. Obes Surg , 14 ,334–340.

surgery. Ann Surg , 248 , 10–5.

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GriffenWO, Printen KJ (eds.). (1987) Surgical Management of Morbid Obesity. Marcel

Guidone C, Manco M, Valera-Mora E, et al. (2006) Mechanisms of Recovery from Type 2 Diabetes after Malabsorptive Bariatric Surgery. Diabetes,55, 2025–2031. Gumbs AA, Pomp A, Gagner M. (2007) Revisional bariatric surgery for inadequate weight

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Keshishian A, Zahriya K, Hartoonian T, et al. (2004) Duodenal switch is a safe operation for patients who have failed other bariatric operations. Obes Surg, 14, 1187–1192. Lee CM, Cirangle PT, Jossart GH; (2007), Vertical gastrectomy for morbid obesity in 216

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Marinari G, Adami GF, Camerini G, et al.(1997). The effect of biliopancreatic diversion on

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Ren CJ, Patterson E, Gagner M. (2000) early results of biliopancreatic diversion with duodenal switch; a case series of 40 consecutive patients. Obes surg, 10 , 514-523. SAGES Guidelines Committee. SAGES guideline for clinical application of laparoscopic

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patients with morbid obesity before and after biliopancreatic bypass. Atheroscl

and Normal Acute Insulin Response to Glucose in Obese Subjects with Type 2

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Diabetes Following Bariatric Surgery. Diabetes, 52 ,1098–1103.

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Genoa, Italy, September, 1987.

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(BPD). In: Proceedings of the Third International Symposium on Obesity Surgery.

**9**

*Brazil*

**Body Weight and Energy Intake**

**and Expenditure in Bariatric Surgery**

 Karina Rodrigues Quesada, Carolina Leandro de Souza, Irineu Rasera Junior and Celso Vieira de Souza Leite *UNESP - Universidade Estadual Paulista – Botucatu-SP,*

*Clinica Bariátrica – Hospital dos Fornecedores de Cana, Piracicaba-SP,*

Body weight is ultimately determined by energy homeostasis, a complex process of regulation. Homeostasis is one of the greatest challenges for understanding the etiology, treatment and prevention of obesity (Hill, 2006). The high rate of weight regain in individuals who undergo weight loss treatments is proof of this (Melo et al., 2008). Even among morbidly obese individuals submitted to more radical treatments, such as surgery, weight regain sometimes occurs [Fogaça, 2009]. In this sense, energy intake and expenditure assessments represent extremely important factors, both for studies and as an aid in the

Given the premise that all obesity treatment methods are based on reducing food intake and increasing energy metabolism, the present chapter intends to discuss the variables in the energy balance equation using the results from works of the research group *Bariatric Surgery and Metabolism* of Paulista State University – UNESP, Campus Botucatu, São Paulo, Brazil, and of the Bariatric C.inic of Piracicaba, São Paulo, Brazil, as reference. Components of

Indirect calorimetry is a reference method that has been used for almost 100 years for measuring energy intake in humans during resting or physical activity. Studies using indirect calorimetry allow assessing the effects of energy intake, physical activity and other factors involved in the energy metabolism on the total body mass of obese individuals or its compartments. Here, indirect calorimetry was used to assess the agreement between itself and prediction formulas, to discuss the effects of food restriction and to assess energy intake underreporting by obese women submitted to food intake surveys. Indirect calorimetry data also allow one to discuss the effects of weight loss and body mass index on energy expenditure and biochemical indicators of glucose and fat metabolism. These studies allowed the elucidation of some energy metabolism particularities of individuals who undergo bariatric surgery, as well as the proposition of

energy metabolism and indirect calorimetry will be discussed.

**1. Introduction**

process of caring for the obese.

some hypotheses for new studies.

Maria Rita Marques de Oliveira, Patrícia Fátima Sousa Novais,

### **Body Weight and Energy Intake and Expenditure in Bariatric Surgery**

Maria Rita Marques de Oliveira, Patrícia Fátima Sousa Novais, Karina Rodrigues Quesada, Carolina Leandro de Souza, Irineu Rasera Junior and Celso Vieira de Souza Leite *UNESP - Universidade Estadual Paulista – Botucatu-SP, Clinica Bariátrica – Hospital dos Fornecedores de Cana, Piracicaba-SP, Brazil*

#### **1. Introduction**

210 Advanced Bariatric and Metabolic Surgery

Wickremesekera K, Miller G, Naotunne TD, et al. (2005) Loss of Insulin Resistance after

Williams JA: (1964) Effects of upper gastro-intestinal surgery on blood formation and bone

Xu G, Stoffers DA, Habener JF, et al. (1999) . Exendin-4 Stimulates Both Beta-cell Replication and Neogenesis, Resulting in Increased Beta-cell Mass. Diabetes ,48 , 2270–2276.

481.

metabolism. Br J Surg , 51 , 125–134.

Roux-en-Y Gastric Bypass Surgery: A Time Course Study. Obes Surg ,15 , 474–

Body weight is ultimately determined by energy homeostasis, a complex process of regulation. Homeostasis is one of the greatest challenges for understanding the etiology, treatment and prevention of obesity (Hill, 2006). The high rate of weight regain in individuals who undergo weight loss treatments is proof of this (Melo et al., 2008). Even among morbidly obese individuals submitted to more radical treatments, such as surgery, weight regain sometimes occurs [Fogaça, 2009]. In this sense, energy intake and expenditure assessments represent extremely important factors, both for studies and as an aid in the process of caring for the obese.

Given the premise that all obesity treatment methods are based on reducing food intake and increasing energy metabolism, the present chapter intends to discuss the variables in the energy balance equation using the results from works of the research group *Bariatric Surgery and Metabolism* of Paulista State University – UNESP, Campus Botucatu, São Paulo, Brazil, and of the Bariatric C.inic of Piracicaba, São Paulo, Brazil, as reference. Components of energy metabolism and indirect calorimetry will be discussed.

Indirect calorimetry is a reference method that has been used for almost 100 years for measuring energy intake in humans during resting or physical activity. Studies using indirect calorimetry allow assessing the effects of energy intake, physical activity and other factors involved in the energy metabolism on the total body mass of obese individuals or its compartments. Here, indirect calorimetry was used to assess the agreement between itself and prediction formulas, to discuss the effects of food restriction and to assess energy intake underreporting by obese women submitted to food intake surveys. Indirect calorimetry data also allow one to discuss the effects of weight loss and body mass index on energy expenditure and biochemical indicators of glucose and fat metabolism. These studies allowed the elucidation of some energy metabolism particularities of individuals who undergo bariatric surgery, as well as the proposition of some hypotheses for new studies.

Body Weight and Energy Intake and Expenditure in Bariatric Surgery 213

The labeled elements are then measured in organic fluids, namely blood and urine. The equations for predicting the energy requirements proposed by the Institute of Medicine (2005) in the Dietary Reference Intakes (DRI) stemmed from studies using doubly-labeled water in normal weight, pre-obese and obese populations. Studies with doubly-labeled water have made the generalized low-metabolism hypothesis associated with obesity less

Many researchers have observed that obese individuals, contrary to the expected, present a high REE, that is, their metabolic rate is not low (Das et al., 2004; Prentice, 2007). Obese individuals present a higher amount of lean mass, the main REE determinant (Prentice et al., 1986; Prentice, 2007; Ravussin et al., 1986). The occurrence of less energy expenditure in other components of the energy metabolism has also been studied in obese individuals. Danforth (1985) noticed reduced thermogenesis from foods. Other authors have showed that REE is influenced by regular physical activity, diet, blood pressure, as well as hormones and cytokines (Trayhurn et al., 1995; Hardie et al., 1996). Genetic predisposition must also be

Many genes of the molecular components of physiological systems that regulate energy balance are involved in obesity (Duarte et al., 2007; Yurtcu et al., 2009). Examples of this are the polymorphisms found in genes of the uncoupling proteins 2 and 3 (UCP2 and UCP3) and in leptin receptors (LEPR) (Jacobson et al., 2006). Polymorphism Gln223Arg of the gene LEPR, for example, has already been associated with obesity in a sample of the Brazilian population, and it presented a strong association with body mass index – BMI (Duarte et al., 2007). Studies with rats show that leptin can reduce adiposity both by promoting changes in eating habits and by increasing energy expenditure (Halaas et al., 1995). Ghrelin, a gastric peptide involved in the regulation of satiety and oxidation of energy substrates, is of interest for genetic studies on the weight loss mechanisms promoted by bariatric surgery (Marzullo et al., 2004). The regulation of ghrelin effects on hypothalamic neurons has been suggested as the most important mechanism by which leptin controls energy intake and body weight

In some people, low energy expenditure could be explained by adaptive thermogenesis, which would occur naturally or as a consequence of dietary restrictions. There is evidence that low energy intake is a predictor of weight gain and that, in individuals who undergo weight loss therapies, decreased REE is associated with weight regain over time (Doucet et al. 2000). In this sense, food restriction promotes adaptive physiological mechanisms that serve as a defense of the body to maintain body weight, resulting in less energy expenditure (Negrão & Licino, 2000). Hence, food restriction produces weight loss under adaptive conditions. The Institute of Medicine (2005), in the energy DRI assumes a reduction of 7.2 Kcal for each lost gram, which corresponds to 16.6 Kcal of TEE reduction at each kilogram lost. Furthermore, it considers a reduction of 8.4% of the TEE after 10 weeks of food restriction because of the adaptation to food restriction. In our studies, we have observed that in fact there is not a linear relationship between energy intake and body weight homeostasis. As shown by Figure 1, there is no correlation between total dietary energy and weight loss among obese women but there is a weak correlation between the reduced proportion of the total energy (TE) intake. This shows how relevant it is to personalize the diet plan considering the adaptation of the energy metabolism to restrictive diets. Caution is also warranted when prescribing excessively restrictive diets. Another relevant finding of our study group that corroborates this statement

evident.

(Sahu, 2004).

considered a determinant of energy expenditure.

#### **2. Energy expenditure and food restriction**

Daily total energy expenditure (TEE) is the term used for defining the amount of energy necessary for an organism to perform its vital functions and activities of daily living. TEE consists of the resting energy expenditure (REE), which is the energy used by the body during rest, that is, in bed, under comfortable environmental conditions (60-75% do TEE), by food-induced thermogenesis, which is the heat effect of foods (5-15% do GET) and by energy spent on physical activities, considered the most variable component of the TEE and which can contribute to a significant amount of the energy spent by very active individuals (Meirelles & Gomes, 2004, Prentice, 2007).

Indirect calorimetry is a noninvasive technique used to measure the volume and concentration of the gases inhaled by the lungs and allows the calculation of the amount of oxygen (O2) consumed and the production of carbonic gas (CO2). These values may stem from the baseline energy expenditure (BEE), the REE and the respiratory quotient (RQ), given by the equation: exhaled CO2 /inhaled O2 (Simyrnios & Curley, as in Rippe et al., 1996). There is a difference between BEE and REE. The BEE corresponds to the energy expenditure that occurs during a 12- to 14-hour fast and with the individual resting in the supine position, awake and immobile, under comfortable environmental conditions. This standardized metabolic state corresponds to the situation in which foods and physical activity have the least influence on metabolism (Institute of Medicine, 2005). Meanwhile, REE is obtained while the individual is awake in the supine position and includes the energy used during awakeness plus the energy used for food metabolism, or thermogenesis (Institute of Medicine, 2005). Both BEE and REE are influenced by gender, age, nutritional status and endocrine problems.

Thermogenesis, or thermal effect of foods, corresponds to the increase in energy expenditure after food intake for digestion to occur and for the substrates to be transformed and stored. It represents roughly 5 to 10% of the TEE (Institute of Medicine, 2005; Prentice, 2007). Thermogenesis intensity and duration are determined primarily by the amount and composition of the foods consumed (Flatt, as cited in Bray, 1978). The use of proteins demands more energy than the use of carbohydrates, which demands more energy than the use of fats (Institute of Medicine, 2005, 1998, Larson et al., 1995). High-fat diets promote a low RQ. For carbohydrates, the RQ equals 1.00; for proteins, 0.82; and for fats, 0.70. For mixed diets, the RQ of 0.85 is usually used (Rosado & Monteiro, 2001).

Physical activity is the most variable component of energy expenditure, varying both from individual to individual and from one day to the next. In inactive individuals, it represents roughly 15% of the TEE, while in active individuals it may exceed 30% of the TEE (World Health Organization, 1998). Physical activity can lead to steep increases in TEE because of the energy cost to perform the exercise and to recover from the exercise, or in the long-term, by changing the REE by increasing the amount of lean mass (Hill et al., 1995). The level of physical activity is commonly described as the ratio between TEE and REE (TEE:REE). This ratio is known as the level of physical activity level (PAL) and is used to asses physical activity habits as a component of daily energy expenditure (Institute of Medicine, 2005).

The doubly-labeled water with deuterium and oxygen-18 technique, although less accessible, has been used increasingly for TEE assessment. The method, based on the principle of isotope dilution, consists in the ingestion of water containing ²H2O and H2 18O.

Daily total energy expenditure (TEE) is the term used for defining the amount of energy necessary for an organism to perform its vital functions and activities of daily living. TEE consists of the resting energy expenditure (REE), which is the energy used by the body during rest, that is, in bed, under comfortable environmental conditions (60-75% do TEE), by food-induced thermogenesis, which is the heat effect of foods (5-15% do GET) and by energy spent on physical activities, considered the most variable component of the TEE and which can contribute to a significant amount of the energy spent by very active individuals

Indirect calorimetry is a noninvasive technique used to measure the volume and concentration of the gases inhaled by the lungs and allows the calculation of the amount of oxygen (O2) consumed and the production of carbonic gas (CO2). These values may stem from the baseline energy expenditure (BEE), the REE and the respiratory quotient (RQ), given by the equation: exhaled CO2 /inhaled O2 (Simyrnios & Curley, as in Rippe et al., 1996). There is a difference between BEE and REE. The BEE corresponds to the energy expenditure that occurs during a 12- to 14-hour fast and with the individual resting in the supine position, awake and immobile, under comfortable environmental conditions. This standardized metabolic state corresponds to the situation in which foods and physical activity have the least influence on metabolism (Institute of Medicine, 2005). Meanwhile, REE is obtained while the individual is awake in the supine position and includes the energy used during awakeness plus the energy used for food metabolism, or thermogenesis (Institute of Medicine, 2005). Both BEE and REE are influenced by gender, age, nutritional

Thermogenesis, or thermal effect of foods, corresponds to the increase in energy expenditure after food intake for digestion to occur and for the substrates to be transformed and stored. It represents roughly 5 to 10% of the TEE (Institute of Medicine, 2005; Prentice, 2007). Thermogenesis intensity and duration are determined primarily by the amount and composition of the foods consumed (Flatt, as cited in Bray, 1978). The use of proteins demands more energy than the use of carbohydrates, which demands more energy than the use of fats (Institute of Medicine, 2005, 1998, Larson et al., 1995). High-fat diets promote a low RQ. For carbohydrates, the RQ equals 1.00; for proteins, 0.82; and for fats, 0.70. For

Physical activity is the most variable component of energy expenditure, varying both from individual to individual and from one day to the next. In inactive individuals, it represents roughly 15% of the TEE, while in active individuals it may exceed 30% of the TEE (World Health Organization, 1998). Physical activity can lead to steep increases in TEE because of the energy cost to perform the exercise and to recover from the exercise, or in the long-term, by changing the REE by increasing the amount of lean mass (Hill et al., 1995). The level of physical activity is commonly described as the ratio between TEE and REE (TEE:REE). This ratio is known as the level of physical activity level (PAL) and is used to asses physical activity habits as a component of daily energy expenditure (Institute of Medicine, 2005).

The doubly-labeled water with deuterium and oxygen-18 technique, although less accessible, has been used increasingly for TEE assessment. The method, based on the principle of isotope dilution, consists in the ingestion of water containing ²H2O and H2

18O.

mixed diets, the RQ of 0.85 is usually used (Rosado & Monteiro, 2001).

**2. Energy expenditure and food restriction**

(Meirelles & Gomes, 2004, Prentice, 2007).

status and endocrine problems.

The labeled elements are then measured in organic fluids, namely blood and urine. The equations for predicting the energy requirements proposed by the Institute of Medicine (2005) in the Dietary Reference Intakes (DRI) stemmed from studies using doubly-labeled water in normal weight, pre-obese and obese populations. Studies with doubly-labeled water have made the generalized low-metabolism hypothesis associated with obesity less evident.

Many researchers have observed that obese individuals, contrary to the expected, present a high REE, that is, their metabolic rate is not low (Das et al., 2004; Prentice, 2007). Obese individuals present a higher amount of lean mass, the main REE determinant (Prentice et al., 1986; Prentice, 2007; Ravussin et al., 1986). The occurrence of less energy expenditure in other components of the energy metabolism has also been studied in obese individuals. Danforth (1985) noticed reduced thermogenesis from foods. Other authors have showed that REE is influenced by regular physical activity, diet, blood pressure, as well as hormones and cytokines (Trayhurn et al., 1995; Hardie et al., 1996). Genetic predisposition must also be considered a determinant of energy expenditure.

Many genes of the molecular components of physiological systems that regulate energy balance are involved in obesity (Duarte et al., 2007; Yurtcu et al., 2009). Examples of this are the polymorphisms found in genes of the uncoupling proteins 2 and 3 (UCP2 and UCP3) and in leptin receptors (LEPR) (Jacobson et al., 2006). Polymorphism Gln223Arg of the gene LEPR, for example, has already been associated with obesity in a sample of the Brazilian population, and it presented a strong association with body mass index – BMI (Duarte et al., 2007). Studies with rats show that leptin can reduce adiposity both by promoting changes in eating habits and by increasing energy expenditure (Halaas et al., 1995). Ghrelin, a gastric peptide involved in the regulation of satiety and oxidation of energy substrates, is of interest for genetic studies on the weight loss mechanisms promoted by bariatric surgery (Marzullo et al., 2004). The regulation of ghrelin effects on hypothalamic neurons has been suggested as the most important mechanism by which leptin controls energy intake and body weight (Sahu, 2004).

In some people, low energy expenditure could be explained by adaptive thermogenesis, which would occur naturally or as a consequence of dietary restrictions. There is evidence that low energy intake is a predictor of weight gain and that, in individuals who undergo weight loss therapies, decreased REE is associated with weight regain over time (Doucet et al. 2000). In this sense, food restriction promotes adaptive physiological mechanisms that serve as a defense of the body to maintain body weight, resulting in less energy expenditure (Negrão & Licino, 2000). Hence, food restriction produces weight loss under adaptive conditions. The Institute of Medicine (2005), in the energy DRI assumes a reduction of 7.2 Kcal for each lost gram, which corresponds to 16.6 Kcal of TEE reduction at each kilogram lost. Furthermore, it considers a reduction of 8.4% of the TEE after 10 weeks of food restriction because of the adaptation to food restriction. In our studies, we have observed that in fact there is not a linear relationship between energy intake and body weight homeostasis. As shown by Figure 1, there is no correlation between total dietary energy and weight loss among obese women but there is a weak correlation between the reduced proportion of the total energy (TE) intake. This shows how relevant it is to personalize the diet plan considering the adaptation of the energy metabolism to restrictive diets. Caution is also warranted when prescribing excessively restrictive diets. Another relevant finding of our study group that corroborates this statement

Body Weight and Energy Intake and Expenditure in Bariatric Surgery 215

(2010) assessed 27 prediction equations in relation to the indirect calorimetry data from Belgium women and concluded that more specific equations are necessary for women

Chart 1. Energy expenditure determined by indirect calorimetry in women recruited in

Fig. 2. **Comparison of the resting energy expenditure measured by indirect calorimetry (IC) and estimated by different equation in women after two years of bariatric surgery** (HB= Harris & Benedict; p<0.01 means compared with ANOVA; \*p<0.01 others compared with the Tukey test; \*\*p<0.05 in the comparison with FAO 1 and Luis by the Tukey test).

The metabolic state can be classified as normal, high or low, by comparing the measured REE with the estimated REE according to the mean of a reference population, using a variation coefficient of 15% (Food and Agriculture Organization, World Health Organization & Organização das Nações Unidas, 1985). In this sense, very low REE values deserve better

These equations are based on body mass, height, age, gender and specific body composition markers, such as body surface area, lean mass, fat mass, total body potassium, among others (Rocha et al., 2005). The equations have been used in underweight, overweight, obese and morbidly obese individuals and also in those with specific diseases. However, interpersonal

investigations regarding adaptation to metabolic restriction after bariatric surgery.

REE Mean±SD REE/BW

< 25 22 1216±214 22±3 Dallemole, 2006 25-30 11 1322±212 23±3 Dallemole, 2006 30-35 13 1425±167 19±3 Dallemole, 2006 > 35 35 1600±430 16±4 Souza, 2006

46±6 21 2006±376 17±4 Cesar et al., 2008 39±6 21 1763±310 18±3 César et al., 2008

< 30 18 1046±264 15±4 Fogaça, 2009 > 30 27 1270±252 15±3 Fogaça, 2009

Mean±SD Reference

Kg/m2 <sup>n</sup>

whose BMI > 30 Kg/m2.

Surgery-naive

after surgery

surgery

Before and 3 months

2 or more years after

Piracicaba, São Paulo, Brazil.

Population BMI

was that there is a negative correlation between the reported number of attempts of losing weight and the resting energy expenditure measured by indirect calorimetry, assessed in 100 women in the waiting line for bariatric surgery.

Fig. 1. Correlation between the absolute value (left) and the proportion of reduction of the habitually consumed energy in obese women after 2 months of a low-calorie diet (n = 28). SPEARMAN and RANK tests, with probability considered significant when p < 0.05.

In studies done in the region of Piracicaba, São Paulo, Brazil (Dallemole, 2006; Souza, 2006; Fogaça, 2009) with women recruited from the general population and those who had undergone bariatric surgery, as shown in Chart 1, energy expenditure increases with body weight. However, in relative terms, there is less energy expenditure by unit of weight as weight increases. Operated women present absolute and relative REE lower than the other women.

Since the first equation proposed by Harris and Benedict in 1919, many equations to predict REE were developed based on indirect calorimetry, and also to estimate TEE by combining the expenditure with physical activities with REE. The formulas used for predicting energy requirements have been widely used in clinical practice.

A cross-sectional study was done by our group with 51 women aged from 28 to 61 years submitted to banded or not bariatric surgery (Roux-en-Y gastric bypass, RYGB) 5.1±1.7 years before the study, all of them with stable weight. The measured REE was confronted with the values of the respective predictive equations obtained from regression studies in a number of different populations (Harris & Benedict, 1919; Schofield, 1985; Food and Agriculture Organization, World Health Organization & Organização das Nações Unidas, 1985; Owen et al., 1986; Mifflin et al., 1990, Luis et al., 2006). When the measurements were compared (Figure 2), the values obtained by indirect calorimetry were below those obtained by the equations, and when the results were organized in increasing order of the value obtained by calorimetry (Figure 3), there was great similarity in the behavior of the lines constructed with the sequence of the results of the equations, but they diverged from those constructed with the results of calorimetry. Thirty-one (77.5%) women presented a median REE measured by indirect calorimetry below the REE estimated by the Harris & Benedict (1919) equation, indicating some women in the group had low metabolism. Weijs & Vansant

was that there is a negative correlation between the reported number of attempts of losing weight and the resting energy expenditure measured by indirect calorimetry, assessed in 100

80

%

60

40

20

0

Fig. 1. Correlation between the absolute value (left) and the proportion of reduction of the habitually consumed energy in obese women after 2 months of a low-calorie diet (n = 28). SPEARMAN and RANK tests, with probability considered significant when p < 0.05.

In studies done in the region of Piracicaba, São Paulo, Brazil (Dallemole, 2006; Souza, 2006; Fogaça, 2009) with women recruited from the general population and those who had undergone bariatric surgery, as shown in Chart 1, energy expenditure increases with body weight. However, in relative terms, there is less energy expenditure by unit of weight as weight increases. Operated women present absolute and relative REE lower than the other

Since the first equation proposed by Harris and Benedict in 1919, many equations to predict REE were developed based on indirect calorimetry, and also to estimate TEE by combining the expenditure with physical activities with REE. The formulas used for predicting energy

A cross-sectional study was done by our group with 51 women aged from 28 to 61 years submitted to banded or not bariatric surgery (Roux-en-Y gastric bypass, RYGB) 5.1±1.7 years before the study, all of them with stable weight. The measured REE was confronted with the values of the respective predictive equations obtained from regression studies in a number of different populations (Harris & Benedict, 1919; Schofield, 1985; Food and Agriculture Organization, World Health Organization & Organização das Nações Unidas, 1985; Owen et al., 1986; Mifflin et al., 1990, Luis et al., 2006). When the measurements were compared (Figure 2), the values obtained by indirect calorimetry were below those obtained by the equations, and when the results were organized in increasing order of the value obtained by calorimetry (Figure 3), there was great similarity in the behavior of the lines constructed with the sequence of the results of the equations, but they diverged from those constructed with the results of calorimetry. Thirty-one (77.5%) women presented a median REE measured by indirect calorimetry below the REE estimated by the Harris & Benedict (1919) equation, indicating some women in the group had low metabolism. Weijs & Vansant

0 2 4 6 8 10 12 14 16

r = 0,321 p = 0,05 n = 28

redução da massa corporal (kg)

Weight loss (kg)

Intake (Kcal) Intake Reduction (%)

r = 0,197 NS n = 28

women in the waiting line for bariatric surgery.

women.

0 2 4 6 8 10 12 14 16

redução da massa corporal (kg)

Weight loss (kg)

requirements have been widely used in clinical practice.

Chart 1. Energy expenditure determined by indirect calorimetry in women recruited in Piracicaba, São Paulo, Brazil.

The metabolic state can be classified as normal, high or low, by comparing the measured REE with the estimated REE according to the mean of a reference population, using a variation coefficient of 15% (Food and Agriculture Organization, World Health Organization & Organização das Nações Unidas, 1985). In this sense, very low REE values deserve better investigations regarding adaptation to metabolic restriction after bariatric surgery.

These equations are based on body mass, height, age, gender and specific body composition markers, such as body surface area, lean mass, fat mass, total body potassium, among others (Rocha et al., 2005). The equations have been used in underweight, overweight, obese and morbidly obese individuals and also in those with specific diseases. However, interpersonal

Body Weight and Energy Intake and Expenditure in Bariatric Surgery 217

Possible error sources can distort information about food intake, such as the perception of what is eaten, the interviewee's memory, the effects stemming from age, gender and interview environment, daily diet variation and seasonality, submission to data collection can affect the intake pattern and veracity of the information, the ability of the interviewer to obtain information and the disposition to collaborate with the investigation (Witschi, as in Willett, 1990). Practically, all dietary assessment studies are based on self-reporting of food intake, which can be biased, resulting in under- or overreporting of real energy intake (Black et al., 1991; Black, 2000), being able to seriously distort the interpretation of the study results

Underreporting has been associated with a number of different individual characteristics, including gender, body mass index, age, ethnicity, race, smoking, education level, social class, depression and physical activity (Johansson, et al., 2001; Scagliusi, et al., 2003; Scagliusi et al., 2008; Maurer et al., 2006, Maurer et al., 2008; Mendez et al., 2011). The desire to be socially accepted and body dissatisfaction have also been associated with underreporting of food intake (Tooze et al., 2004; Maurer et al., 2006; Scagliusi, 2007). Excess weight may be one of the greatest determinants of subnotification (Johansson et al., 2001;

In individuals who are in energy balance, energy intake should correspond to the TEE. Thus, the doubly labeled water can be used to validate the energy obtained through dietary surveys. However, this method is unviable in large studies because of its cost and because it is technically challenging for use in routine validation of energy intake (Schoeller, 1999;

As an alternative, other methods for identifying underreporting can be used, such as the comparison between reported energy intake (EIrep) with TEE, when both are expressed in multiples of the REE, using a confidence interval for statistically comparing EIrep:REE with the level of PAL. During weight stabilization, EIrep:REE theoretically is equal to TEE:REE. The ratio TEE:REE is also known as PAL, then the equation may be rewritten as EIrep:REE =

As described by Black 2000, the cut-off point of the ratio EIrep:REE should be calculated for the group being studied, since below this level it is statistically unlikely that the mean energy intake reported represents the real consumption, according to the equation below:

> (S /100) Cut off point PAL exp [ SD ] <sup>n</sup>

Where SD is the standard deviation. When 95% of the confidence interval is used (SD min =-2) or 99.7% (SD min = - 3); **n** is the number of individuals in the study, but when this formula is used to individually detect underreporting, n=1. **S** is the factor that takes into consideration

EIrep 2 2

Where VCEIrep is the intra-individual energy intake variation coefficient; **d** is the number of days that the survey was administered; VCREE is the intra-individual variation coefficient of

S CV CV

the variation of all components of the equation and is given by:

2

d

CV

min

REE PAL

Johnson, 2002; Huang, et al., 2005; Bazanelli et al., 2010).

(Rennie et al., 2006).

Livingstone & Black, 2003).

PAL (Goldberg, et al., 1991).

variation shows that much caution is necessary for estimating REE by the existing prediction equations, since it has been shown that they do not always estimate REE correctly (Frankenfield & Yousey, 2005) resulting in errors when estimating the energy requirements of individuals and populations (Duarte et al., 2007). More studies are necessary to state if the proportion of women with low metabolism who underwent bariatric surgery was in fact greater than that of the surgery-naive population, obese or otherwise, since there are not enough data from the population who lives in the same environmental conditions as that of the present study.

Although much has been done since Harris & Benedict (1919), the current formulas for estimating REE and TEE (that takes into account the energy spent in physical activities) are very limited and tend to overestimate the results.

Fig. 3. Illustration of the resting energy expenditure, in increasing order, measured by indirect calorimetry (IC), in relation to that estimated by different equations among women two years or more after bariatric surgery (n=51).

#### **3. Energy intake**

One of the most challenging aspects of the science and practice of nutrition and dietetics is the measurement of energy and nutrient intakes, given the limitations of the methods to correctly measure food intake (Subar et al., 2006). Dietary surveys are used as indirect methods for assessing nutritional status. However, these instruments are subject to mistakes inherent to the individual and data analysis and use (Beaton, 1994; Slater et al., 2004). Individual quantitative and qualitative food intake may be estimated by different diet survey methods. There are retrospective methods where individuals recall the foods they have eaten, such as the Food Frequency Questionnaire (FFQ) and the 24-hour Recall (24hR). And the methods in which the individual records, when he eats, all the foods he ate, thereby creating a food diary (Gibson, 2005).

Intraindividual error sources, because of the variability of the food intake pattern, or interindividual error sources, stemming from the distribution of the population's requirements, together with a small number of days of observation, have a great impact on the reliability of food intake data analysis (Nusser et al., 1996). Hence, intake assessment studies will always be reporting the apparent intake of the individual and not the real intake, but they can be statistically adjusted to approximate the actual intake (Institute of Medicine, 2005).

variation shows that much caution is necessary for estimating REE by the existing prediction equations, since it has been shown that they do not always estimate REE correctly (Frankenfield & Yousey, 2005) resulting in errors when estimating the energy requirements of individuals and populations (Duarte et al., 2007). More studies are necessary to state if the proportion of women with low metabolism who underwent bariatric surgery was in fact greater than that of the surgery-naive population, obese or otherwise, since there are not enough data from the population who lives in the same environmental conditions as that of

Although much has been done since Harris & Benedict (1919), the current formulas for estimating REE and TEE (that takes into account the energy spent in physical activities) are

Fig. 3. Illustration of the resting energy expenditure, in increasing order, measured by indirect calorimetry (IC), in relation to that estimated by different equations among women

One of the most challenging aspects of the science and practice of nutrition and dietetics is the measurement of energy and nutrient intakes, given the limitations of the methods to correctly measure food intake (Subar et al., 2006). Dietary surveys are used as indirect methods for assessing nutritional status. However, these instruments are subject to mistakes inherent to the individual and data analysis and use (Beaton, 1994; Slater et al., 2004). Individual quantitative and qualitative food intake may be estimated by different diet survey methods. There are retrospective methods where individuals recall the foods they have eaten, such as the Food Frequency Questionnaire (FFQ) and the 24-hour Recall (24hR). And the methods in which the individual records, when he eats, all the foods he ate, thereby

Intraindividual error sources, because of the variability of the food intake pattern, or interindividual error sources, stemming from the distribution of the population's requirements, together with a small number of days of observation, have a great impact on the reliability of food intake data analysis (Nusser et al., 1996). Hence, intake assessment studies will always be reporting the apparent intake of the individual and not the real intake, but they can be statistically adjusted to approximate the actual intake (Institute of

the present study.

**3. Energy intake**

Medicine, 2005).

very limited and tend to overestimate the results.

two years or more after bariatric surgery (n=51).

creating a food diary (Gibson, 2005).

Possible error sources can distort information about food intake, such as the perception of what is eaten, the interviewee's memory, the effects stemming from age, gender and interview environment, daily diet variation and seasonality, submission to data collection can affect the intake pattern and veracity of the information, the ability of the interviewer to obtain information and the disposition to collaborate with the investigation (Witschi, as in Willett, 1990). Practically, all dietary assessment studies are based on self-reporting of food intake, which can be biased, resulting in under- or overreporting of real energy intake (Black et al., 1991; Black, 2000), being able to seriously distort the interpretation of the study results (Rennie et al., 2006).

Underreporting has been associated with a number of different individual characteristics, including gender, body mass index, age, ethnicity, race, smoking, education level, social class, depression and physical activity (Johansson, et al., 2001; Scagliusi, et al., 2003; Scagliusi et al., 2008; Maurer et al., 2006, Maurer et al., 2008; Mendez et al., 2011). The desire to be socially accepted and body dissatisfaction have also been associated with underreporting of food intake (Tooze et al., 2004; Maurer et al., 2006; Scagliusi, 2007). Excess weight may be one of the greatest determinants of subnotification (Johansson et al., 2001; Johnson, 2002; Huang, et al., 2005; Bazanelli et al., 2010).

In individuals who are in energy balance, energy intake should correspond to the TEE. Thus, the doubly labeled water can be used to validate the energy obtained through dietary surveys. However, this method is unviable in large studies because of its cost and because it is technically challenging for use in routine validation of energy intake (Schoeller, 1999; Livingstone & Black, 2003).

As an alternative, other methods for identifying underreporting can be used, such as the comparison between reported energy intake (EIrep) with TEE, when both are expressed in multiples of the REE, using a confidence interval for statistically comparing EIrep:REE with the level of PAL. During weight stabilization, EIrep:REE theoretically is equal to TEE:REE. The ratio TEE:REE is also known as PAL, then the equation may be rewritten as EIrep:REE = PAL (Goldberg, et al., 1991).

As described by Black 2000, the cut-off point of the ratio EIrep:REE should be calculated for the group being studied, since below this level it is statistically unlikely that the mean energy intake reported represents the real consumption, according to the equation below:

$$\text{Cut} - \text{off} \text{ point} = \text{PAL} \times \exp\left[\text{SD}\_{\text{min}} \times \frac{\text{(S} / 100)}{\sqrt{\text{n}}}\right]$$

Where SD is the standard deviation. When 95% of the confidence interval is used (SD min =-2) or 99.7% (SD min = - 3); **n** is the number of individuals in the study, but when this formula is used to individually detect underreporting, n=1. **S** is the factor that takes into consideration the variation of all components of the equation and is given by:

$$\mathbf{S} = \sqrt{\left[ \left( \frac{\mathbf{C} \mathbf{V}^2\_{\mathrm{Hrep}}}{\mathbf{d}} \right) + \left( \mathbf{C} \mathbf{V}^2\_{\mathrm{REE}} \right) + \left( \mathbf{C} \mathbf{V}^2\_{\mathrm{PAL}} \right) \right]}$$

Where VCEIrep is the intra-individual energy intake variation coefficient; **d** is the number of days that the survey was administered; VCREE is the intra-individual variation coefficient of

Body Weight and Energy Intake and Expenditure in Bariatric Surgery 219

proportion of macronutrients in the energy of the diet varied little.  Those in the waiting line for surgery reported consuming a fat proportion above the recommended proportion (Institute of Medicine, 2005), while the operated women reported consuming a proportion close to the upper limit. About the data presented by Table 1, one may ask how much they correspond to reality based on the analysis presented by Table 2 given the discrepancy between the measured expenditure and reported intake. The data presented in Table 1 were obtained from 24-hour recalls on nonconsecutive days, one of the days being on a weekend. The data in Table 2 stem from indirect calorimetry, and the total energy requirement was calculated by the DRI formula (Institute of Medicine, 2005). Among these women, the EIrep:REE and PAL values that, in theory should agree,

Our data (Table 2 and Figure 3) show that energy intake divided by resting energy expenditure (EIrep:REE) was not compatible with the level of physical activity (PALest) of the studied population. On the other hand, this can be explained by overestimating the reported physical activity which composes the PALest calculation. It may also be related to a substantially greater energy intake than that reported. Although one may not expect absolute agreement on this datum, since there are measurement errors in all elements of the equation (EIrep:REE = PAL). The fact is that the studied women were in a stable weight condition and reported consuming half the estimated energy requirement (RE). This leads us to the generalization that the scale is still the best instrument for assessing the adequacy of energy intake. That is, if the individual is involuntarily gaining weight, it is because he is consuming more energy than he needs. However, it is not convenient to give up trying to solve this difficult issue, which is to know the values of the two sides of this balance, which for now remain obscure. This information can help to explain, for example, weight recovery after bariatric surgery, which, in most cases, is accompanied by intake underreporting.

Fig. 4. **Correlation between the estimated level of physical activity** (PALest) and the ratio Energy Intake/Resting Energy Expenditure (EIrep/REE) in women more than two years

There is a consensus that lean mass (LM) is the greatest determinant of energy expenditure, since it is metabolically more active than fat mass (Ravussin et al., 1986). Meanwhile, the

present only a small correlation (Figure 4)

after bariatric surgery (n=40).

**4. Body mass**

repeated REE measurements and CVPAL is the intra-individual variation coefficient of the level of physical activity.

Recently, other authors (Huang, 2005; Mendez, et al., 2011), assessed the underreporting phenomenon comparing EIrep with estimated TEE using the DRI equations (Institute of Medicine, 2005), adjusting the intra-individual variation of the equation components. The cut-off point is calculated for the study group in percentage (%EI:TEE).

p = Mann Whitney test used for comparing energy and macronutrient intakes before and after surgery Table 1. The energy and macronutrient intakes of women before surgery and two or more years after surgery, Pircacicaba-SP, Brazil.

EIrep = reported energy intake, ER = estimated energy requirement, REE = measured resting energy expenditure, PALest = estimated level of physical activity.

\**p*<0.000 in the paired t-test between EIrep and ER and between Harris & Benedict (1919) and REEmeasured.

Table 2. Energy intake and expenditure variables in women more than two years after bariatric surgery (n=40).

Among the bariatric patients we studied, mean reported energy intake before surgery corresponds to half the intake reported after surgery (Table 1). In the comparison, the

repeated REE measurements and CVPAL is the intra-individual variation coefficient of the

Recently, other authors (Huang, 2005; Mendez, et al., 2011), assessed the underreporting phenomenon comparing EIrep with estimated TEE using the DRI equations (Institute of Medicine, 2005), adjusting the intra-individual variation of the equation components. The

> **Before surgery n=37**

Energy (Kcal) 2780 1037 6338 1346 673 2981 0.000 Carbohydrates (g)<PHONE_NUMBER> 166 68 428 0.000 Fats (g) 110 28 395 51 20 104 0.000 Proteins (g) 104 38 302 51 15 89 0.000

Carbohydrates (%) 50 28 72 51 38 61 0.387 Fats (%) 38 14 56 34 25 49 0.034 Proteins (%) 16 9 23 15 8 25 0.226 p = Mann Whitney test used for comparing energy and macronutrient intakes before and after surgery Table 1. The energy and macronutrient intakes of women before surgery and two or more

median 25% 75% median 25% 75%

**Median First Quartile**

**(25%)**

**After surgery**

**n=35 p**

**Third Quartile (75%)**

cut-off point is calculated for the study group in percentage (%EI:TEE).

**Mean Standard**

**deviation**

EIrep 1428 523 1334 1147 1678 ER 2786\* 524 2812 2389 3036 Harris&Benedict (1919) 1445\* 152 1445 1376 1604 REE 1188 276 1209 1023 1376 PALest 1,45 0,22 1,42 1,28 1,56 EIrep :REE 1,27 0,57 1,08 0,86 1,66 EIrep = reported energy intake, ER = estimated energy requirement, REE = measured resting energy

\**p*<0.000 in the paired t-test between EIrep and ER and between Harris & Benedict (1919) and REEmeasured.

Among the bariatric patients we studied, mean reported energy intake before surgery corresponds to half the intake reported after surgery (Table 1). In the comparison, the

Table 2. Energy intake and expenditure variables in women more than two years after

level of physical activity.

**Energy and macronutrients**

Energy distribution

years after surgery, Pircacicaba-SP, Brazil.

expenditure, PALest = estimated level of physical activity.

bariatric surgery (n=40).

proportion of macronutrients in the energy of the diet varied little.  Those in the waiting line for surgery reported consuming a fat proportion above the recommended proportion (Institute of Medicine, 2005), while the operated women reported consuming a proportion close to the upper limit. About the data presented by Table 1, one may ask how much they correspond to reality based on the analysis presented by Table 2 given the discrepancy between the measured expenditure and reported intake. The data presented in Table 1 were obtained from 24-hour recalls on nonconsecutive days, one of the days being on a weekend. The data in Table 2 stem from indirect calorimetry, and the total energy requirement was calculated by the DRI formula (Institute of Medicine, 2005). Among these women, the EIrep:REE and PAL values that, in theory should agree, present only a small correlation (Figure 4)

Our data (Table 2 and Figure 3) show that energy intake divided by resting energy expenditure (EIrep:REE) was not compatible with the level of physical activity (PALest) of the studied population. On the other hand, this can be explained by overestimating the reported physical activity which composes the PALest calculation. It may also be related to a substantially greater energy intake than that reported. Although one may not expect absolute agreement on this datum, since there are measurement errors in all elements of the equation (EIrep:REE = PAL). The fact is that the studied women were in a stable weight condition and reported consuming half the estimated energy requirement (RE). This leads us to the generalization that the scale is still the best instrument for assessing the adequacy of energy intake. That is, if the individual is involuntarily gaining weight, it is because he is consuming more energy than he needs. However, it is not convenient to give up trying to solve this difficult issue, which is to know the values of the two sides of this balance, which for now remain obscure. This information can help to explain, for example, weight recovery after bariatric surgery, which, in most cases, is accompanied by intake underreporting.

Fig. 4. **Correlation between the estimated level of physical activity** (PALest) and the ratio Energy Intake/Resting Energy Expenditure (EIrep/REE) in women more than two years after bariatric surgery (n=40).

#### **4. Body mass**

There is a consensus that lean mass (LM) is the greatest determinant of energy expenditure, since it is metabolically more active than fat mass (Ravussin et al., 1986). Meanwhile, the

Body Weight and Energy Intake and Expenditure in Bariatric Surgery 221

The total LM in the body is the factor that is most closely associated with leptin concentrations in the blood and so BMI, which is an indirect measurement of body fat, is also strongly and positively associated with the concentration of circulating leptin (Considine et al., 1996; Jeon et al., 2003; Kennedy et al., 1997). In a study done by our research group, the positive correlation between BMI and serum concentration of leptin was confirmed (Figure 5). This study assessed 45 women, of which 27 had less than 10% of weight regain 2 or more years after surgery and 18 presented an appropriate weight

Another theme of interest relative to body composition is the role of FM by itself on the improvement of the comorbidities associated with obesity. Lowering of blood glucose (improvement of diabetes) in morbidly obese individuals after surgery occurs even before an important weight loss has been achieved and has been attributed to the modulation of the gastrointestinal hormonal response which acts in the recovery of the first phase of insulin secretion and improves its peripheral resistance (Polyzogopolou et al., 2003; Cummings et al., 2004). The important association of BMI with insulin and leptin concentrations in nondiabetic operated women (Figure 5) confirms the relevance of body weight reduction and maintenance for obtaining benefits after surgery. There was also a correlation of BMI with glucose concentration in women in the late postoperative period. Among the biochemical markers of lipid metabolism, an association between the concentrations of serum triglycerides with BMI was found, but not with total cholesterol and its fractions. The reduction of serum leptin that accompanies the reduction in body weight after bariatric surgery was inversely associated with the secretion of VLDL in studies of particle kinetics (Magkos, 2010), showing that the triglyceride metabolism has an

Fig. 5. Correlation of the serum leptin concentrations and insulin with body mass index (BMI) in women in the late postoperative period after Roux-en-Y gastric bypass (*n=41,*

Finally, an aspect of great relevance associated with obesity and insulin resistance is the distribution of body fat. Not all obese individual are insulin-resistant, and it has been shown that predominantly abdominal obesity is more strongly associated with insulin resistance. Inflammation of the omental adipose tissue is an important determining factor of insulin

loss.

important relationship with BMI.

*r=0.729; R2=0.531; p = 0.000*), (Fogaça, 2009).

resistance (Hardy, 2011).

differences in the volume of fat mass (FM), age and gender would have little effect on energy expenditure (Ravussin et al., 1986). Much has been discussed if an REE reduction could precede obesity; however, some researchers have rejected this hypothesis (Prentice, 2007). On the contrary, obese individuals present a high REE, that is, they do not have a low metabolism (Das et al., 2004; Hams et al., 2009; Prentice, 2007). This may occur because these individuals present a greater amount of lean mass, main determinant of the REE (Prentice, 2007; Prentice et al., 1986; Ravussin et al., 1986). Libel et al. (1995) assessed the energy expenditure during 24 hours and the REE in obese individuals and individuals who had never been obese in their habitual weights; after gaining 10% of the body weight by consuming a hypercaloric diet; or after losing 10 to 20% of the body weight by consuming a hypocaloric diet. They found that energy expenditure changed in both groups, of obese and nonobese individuals, after the change in the body weight. A 10% increase or reduction in habitual body weight causes an increase or reduction, respectively, of 15% in the 24-hour energy expenditure corrected for body weight. They also verified that TEE presented a positive correlation with LM and FM. The positive correlation between the total body mass of obese individuals and TEE has been explained by the increase in energy necessary for moving this mass (Institute of Medicine, 2005).

Reduction of LM associated with weight loss is also discussed, and that the reduction of LM would result in a reduction of TEE, thus the importance of exercising during weight loss. Tamboli et al. (2010) found a LM loss in the order of 27.8% one year after Roux-em-Y gastric bypass and associated this loss with the reduction of the TEE of these patients. In another study done in obese individuals after weight loss, concomitantly with REE reduction, there was a significant reduction of LM (Hill et al., 1987).

Active individuals present a significantly higher REE than inactive individuals of the same weight (Matzinger et al., 2002). There is the hypothesis that this occurs because of the amount of LM, which is greater in active individuals (Tappy et al., 2003). The REE differences in body weight in many individuals like men, women or athletes normally disappear when REE is considered in relation to LM (Institute of Medicine, 2005).

Based on these studies it is possible to verify that body composition, especially LM, significantly affects REE and TEE, both in obese and nonobese individuals. Current knowledge allows us to state that there is little difference between energy expenditure by unit of body mass of an underweight individual and an obese individual, but there is individual variation in the energy expenditure by unit of body mass of individuals in general, which in practice limits the use of formulas that predict energy requirement. In relation to surgery, studies that use more sensitive methods are needed to confirm the hypothesis that the REE adjusted for LM after surgery does not decrease, by adaptation or modification mechanisms of body composition in LM no matter how long after surgery.

Type of fat tissue also appears to have a strong influence on energy expenditure. White fat tissue, in addition to working as a primary site for energy storage, produces a series of substances that act on many places of the body, modulating the general metabolism.  Meanwhile, brown fat tissue is highly specialized and is capable of regulating energy expenditure by adaptive thermogenesis. This process depends on UCP-1 expression (Cinti et al., 1997).  Much has been discussed if an REE reduction could precede obesity; however, some researchers have rejected this hypothesis (Prentice, 2007). On the contrary, obese individuals present a high REE, that is, they do not have a low metabolism (Das et al., 2004; Hams et al., 2009; Prentice, 2007). This may occur because these individuals present a greater amount of lean mass, main determinant of the REE (Prentice, 2007; Prentice et al., 1986; Ravussin et al., 1986). Libel et al. (1995) assessed the energy expenditure during 24 hours and the REE in obese individuals and individuals who had never been obese in their habitual weights; after gaining 10% of the body weight by consuming a hypercaloric diet; or after losing 10 to 20% of the body weight by consuming a hypocaloric diet. They found that energy expenditure changed in both groups, of obese and nonobese individuals, after the change in the body weight. A 10% increase or reduction in habitual body weight causes an increase or reduction, respectively, of 15% in the 24-hour energy expenditure corrected for body weight. They also verified that TEE presented a positive correlation with LM and FM. The positive correlation between the total body mass of obese individuals and TEE has been explained by the increase in energy necessary for

Reduction of LM associated with weight loss is also discussed, and that the reduction of LM would result in a reduction of TEE, thus the importance of exercising during weight loss. Tamboli et al. (2010) found a LM loss in the order of 27.8% one year after Roux-em-Y gastric bypass and associated this loss with the reduction of the TEE of these patients. In another study done in obese individuals after weight loss, concomitantly with REE reduction, there

Active individuals present a significantly higher REE than inactive individuals of the same weight (Matzinger et al., 2002). There is the hypothesis that this occurs because of the amount of LM, which is greater in active individuals (Tappy et al., 2003). The REE differences in body weight in many individuals like men, women or athletes normally

Based on these studies it is possible to verify that body composition, especially LM, significantly affects REE and TEE, both in obese and nonobese individuals. Current knowledge allows us to state that there is little difference between energy expenditure by unit of body mass of an underweight individual and an obese individual, but there is individual variation in the energy expenditure by unit of body mass of individuals in general, which in practice limits the use of formulas that predict energy requirement. In relation to surgery, studies that use more sensitive methods are needed to confirm the hypothesis that the REE adjusted for LM after surgery does not decrease, by adaptation or modification mechanisms of body composition in LM no matter how long after surgery.

Type of fat tissue also appears to have a strong influence on energy expenditure. White fat tissue, in addition to working as a primary site for energy storage, produces a series of substances that act on many places of the body, modulating the general metabolism.  Meanwhile, brown fat tissue is highly specialized and is capable of regulating energy expenditure by adaptive thermogenesis. This process depends on UCP-1 expression (Cinti et al., 1997). White fat tissue is responsible for most of the leptin produced (Cinti et al., 1997), although the action of this peptide occurs in the hypothalamus,

which is where most of its receptors are found (Schwartz et al., 1996).

disappear when REE is considered in relation to LM (Institute of Medicine, 2005).

moving this mass (Institute of Medicine, 2005).

was a significant reduction of LM (Hill et al., 1987).

The total LM in the body is the factor that is most closely associated with leptin concentrations in the blood and so BMI, which is an indirect measurement of body fat, is also strongly and positively associated with the concentration of circulating leptin (Considine et al., 1996; Jeon et al., 2003; Kennedy et al., 1997). In a study done by our research group, the positive correlation between BMI and serum concentration of leptin was confirmed (Figure 5). This study assessed 45 women, of which 27 had less than 10% of weight regain 2 or more years after surgery and 18 presented an appropriate weight loss.

Another theme of interest relative to body composition is the role of FM by itself on the improvement of the comorbidities associated with obesity. Lowering of blood glucose (improvement of diabetes) in morbidly obese individuals after surgery occurs even before an important weight loss has been achieved and has been attributed to the modulation of the gastrointestinal hormonal response which acts in the recovery of the first phase of insulin secretion and improves its peripheral resistance (Polyzogopolou et al., 2003; Cummings et al., 2004). The important association of BMI with insulin and leptin concentrations in nondiabetic operated women (Figure 5) confirms the relevance of body weight reduction and maintenance for obtaining benefits after surgery. There was also a correlation of BMI with glucose concentration in women in the late postoperative period. Among the biochemical markers of lipid metabolism, an association between the concentrations of serum triglycerides with BMI was found, but not with total cholesterol and its fractions. The reduction of serum leptin that accompanies the reduction in body weight after bariatric surgery was inversely associated with the secretion of VLDL in studies of particle kinetics (Magkos, 2010), showing that the triglyceride metabolism has an important relationship with BMI.

Fig. 5. Correlation of the serum leptin concentrations and insulin with body mass index (BMI) in women in the late postoperative period after Roux-en-Y gastric bypass (*n=41, r=0.729; R2=0.531; p = 0.000*), (Fogaça, 2009).

Finally, an aspect of great relevance associated with obesity and insulin resistance is the distribution of body fat. Not all obese individual are insulin-resistant, and it has been shown that predominantly abdominal obesity is more strongly associated with insulin resistance. Inflammation of the omental adipose tissue is an important determining factor of insulin resistance (Hardy, 2011).

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#### **5. Conclusions**

Energy balance is determined by energy intake and expenditure variables. Among the energy expenditure variables, REE and the expenditure with physical activities are responsible for roughly 90% of the TEE. Based on calorimetry studies, we have noticed that there is an important interpersonal variation in REE of women submitted to bariatric surgery. To know the magnitude of the effect of surgery on REE, we are conducting a prospective study to assess the interpersonal variation before surgery and after different lengths of postoperative time. Another aspect that needs to be better elucidated is the magnitude of the effect of physical exercise on REE in different lengths of postoperative periods.

In the energy requirement assessment, the use of prediction REE formulas does not seem adequate for the bariatric population and should be done with caution.

Physical activity is an important component of total energy expenditure and TEE assessment depends on precise information regarding the type and duration of each activity. As the energy intake registry, the registry of physical activity must be detailed and as close as possible of the real energy intake. This is a challenging task since among the obese, overestimation of the reported intake usually happens.

If, on the one hand, physical activities are usually overestimated, on the other hand, and more strikingly, food intake reports are usually underestimated. Among obese women, intake reports can be below the REEmeasured, which is completely implausible. This observation challenges us in the development of more appropriate methods to assess food intake.

BMI is an important indicator of the result of bariatric surgery and more studies are necessary on the effects of the distribution and type of body fat and the surgery results on the comorbidities associated with obesity.

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Energy balance is determined by energy intake and expenditure variables. Among the energy expenditure variables, REE and the expenditure with physical activities are responsible for roughly 90% of the TEE. Based on calorimetry studies, we have noticed that there is an important interpersonal variation in REE of women submitted to bariatric surgery. To know the magnitude of the effect of surgery on REE, we are conducting a prospective study to assess the interpersonal variation before surgery and after different lengths of postoperative time. Another aspect that needs to be better elucidated is the magnitude of the effect of physical

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If, on the one hand, physical activities are usually overestimated, on the other hand, and more strikingly, food intake reports are usually underestimated. Among obese women, intake reports can be below the REEmeasured, which is completely implausible. This observation

BMI is an important indicator of the result of bariatric surgery and more studies are necessary on the effects of the distribution and type of body fat and the surgery results on

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