help button home button Endocrine Society JCEM
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2006-0557
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shah, M.
Right arrow Articles by Garg, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shah, M.
Right arrow Articles by Garg, A.
Related Collections
Right arrow Metabolism
Right arrow Obesity
The Journal of Clinical Endocrinology & Metabolism Vol. 91, No. 11 4223-4231
Copyright © 2006 by The Endocrine Society

REVIEW

Long-Term Impact of Bariatric Surgery on Body Weight, Comorbidities, and Nutritional Status

Meena Shah, Vinaya Simha and Abhimanyu Garg

Division of Nutrition and Metabolic Diseases (M.S., V.S., A.G.), Department of Internal Medicine (V.S., A.G.), and Center for Human Nutrition (M.S., V.S., A.G.), University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75235-9052; and Department of Kinesiology (M.S.), Texas Christian University, Fort Worth, Texas 76129

Address all correspondence and requests for reprints to: Abhimanyu Garg, M.D., Professor and Chief, Division of Nutrition and Metabolic Diseases, Center for Human Nutrition, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, Texas 75235-9052. E-mail: abhimanyu.garg{at}utsouthwestern.edu.


   Abstract
Top
 Abstract
Introduction
 Long-Term Effect of RYGB...
 Mechanisms for Weight Regain
 Effect of Bariatric Surgery...
 Recommendations
 References
 
Context: The number of patients who undergo Roux-en-Y gastric bypass (RYGB) and gastric banding (GB) surgeries has increased dramatically over the past decade, yet the long-term impact of these surgeries on body weight, comorbidities, and nutritional status remains unclear, as do the mechanisms of weight regain.

Evidence Acquisition: The articles were found via PubMed searches. To review the impact of bariatric surgery on weight maintenance and comorbidities, only articles with a postoperative follow-up of 3 yr or longer were included. The articles on nutritional status had a follow-up of 12 months or longer.

Conclusions: RYGB and GB surgeries lead to substantial weight loss in individuals with morbid obesity. However, significant weight regain occurs over the long term, and according to the only well-designed prospective controlled study, the improvement in comorbidities associated with weight loss mitigates in the long term on weight regain. There is some evidence from a retrospective study that RYGB surgery is associated with a modest decrease in long-term mortality. These results remain to be substantiated by well-designed, long-term, randomized and prospective controlled studies. The mechanisms that lead to weight regain need to be further examined and may include increase in energy intake due to enlargement of stoma and adaptive changes in the levels of gut and adipocyte hormones such as ghrelin and leptin, which regulate energy intake; decrease in physical activity; changes in energy expenditure; and other factors. In addition to weight regain, RYGB surgery is associated with frequent incidence of iron, vitamin B12, folate, calcium, and vitamin D deficiency, which requires regular supplementation and monitoring.


   Introduction
Top
 Abstract
 Introduction
Long-Term Effect of RYGB...
 Mechanisms for Weight Regain
 Effect of Bariatric Surgery...
 Recommendations
 References
 
ACCORDING TO THE National Health and Nutrition Examination Survey conducted in 2003–2004, a staggering proportion (66.3%) of the U.S. adults are overweight or obese [body mass index (BMI) ≥ 25 kg/m2], 32.2% are obese (BMI ≥ 30 kg/m2), and 4.8% are morbidly or severely obese (BMI ≥ 40 kg/m2) (1). In addition, according to another survey, the Behavioral Risk Factor Surveillance System, conducted from 1986 to 2000, the prevalence of severe obesity has increased twice as fast as the prevalence of obesity (2).

Obesity is associated with a number of comorbidities including type 2 diabetes, coronary heart disease, hyperlipidemia, hypertension, sleep apnea, pulmonary dysfunction, ischemic stroke, knee osteoarthritis, gallbladder disease, nonalcoholic steatohepatitis, and certain types of cancer (3, 4). In addition, obesity, specifically severe obesity, markedly lessens life expectancy, especially among younger adults (5).

Diet, exercise, and medical therapy have not been shown to be effective in treating severe obesity in the long term (6, 7). This and the steep rise in prevalence of severe obesity and the introduction of laparoscopic procedures may explain the exponential increase in the number of bariatric surgeries from 13,365 in 1998 to 72,177 in 2002 (8). The various types of bariatric procedures include Roux-en-Y gastric bypass (RYGB), gastric banding (GB), vertical banded gastroplasty (VBG), duodenal switch, biliopancreatic diversion, isolated intestinal bypass, and gastrectomy. Of these, RYGB and GB surgeries are the most commonly performed (9) and will be the focus of this review.

According to a recent metaanalysis on bariatric surgery outcomes (10), the patients who undergo RYGB and GB surgeries lose 61.6 and 47.5% of their excess body weight (actual body weight – expected body weight based on height and gender) respectively, and a majority of patients with diabetes, hyperlipidemia, hypertension, and obstructive sleep apnea experience complete resolution or improvement of these comorbidities. However, most of the studies included in the metaanalysis were uncontrolled case series, and patients were followed up for no more than 2 yr. Emerging data, however, suggest some gradual weight regain and return of comorbidities during the long term (11). Therefore, we review the literature on the impact of RYGB and GB surgeries on long-term maintenance of weight loss and improvement in comorbidities and the factors that may lead to weight regain in these patients. We also review the effect of these surgeries on nutritional status and intolerance.

The articles in this review were found via PubMed search engines. Only studies with a postoperative follow-up period of at least 3 yr and in which the patients had achieved their maximum weight loss were considered in the review of the impact of bariatric surgery on weight maintenance and improvement in comorbidities. To assess the impact of bariatric surgery on nutritional status, only studies that followed up patients for at least 12 months postoperatively were included. Because of limited research, we did not apply any entrance criteria on the articles on mechanisms of weight regain in bariatric surgery patients.


   Long-Term Effect of RYGB and GB Surgeries on Body Weight and Comorbidities
Top
 Abstract
 Introduction
 Long-Term Effect of RYGB...
Mechanisms for Weight Regain
 Effect of Bariatric Surgery...
 Recommendations
 References
 
The majority of the studies were uncontrolled case series (12, 13, 14, 15, 16, 17, 18, 19, 20), two were prospective controlled studies (11, 21), and two were retrospective controlled studies (22, 23) (Table 1Go). The studies usually presented the data on weight loss as percent excess weight loss or percent weight change.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Long-term effect of bariatric surgery on weight loss maintenance, comorbidities, and major end points

 
In the 10-yr, prospective, controlled study by Sjostrom et al. (11), percent weight loss decreased from 38% at yr 1 to 25% at yr 10 in RYGB patients and from 21 to 13%, respectively in GB patients (Fig. 1Go). Body weight increased slightly in the matched controls (Fig. 1Go). The rate of recovery from hypercholesterolemia was not different between the surgery (RYGB, GB, and VBG) and control groups at either 2 or 10 yr, whereas the rate of recovery from hypertriglyceridemia, low levels of high-density lipoprotein (HDL) cholesterol, type 2 diabetes, hypertension, and hyperuricemia was more frequent in the surgery groups than in the control group at both 2 and 10 yr. The rate of recovery from comorbidities in the surgery group was, however, much less impressive at 10 yr than 2 yr (Table 1Go), possibly due to the weight regain over time. The authors also reported a significantly better improvement from baseline in serum insulin, triglycerides, total cholesterol, and HDL cholesterol levels in the RYGB group than the GB group at 10 yr, probably because the RYGB patients had a higher percent weight loss than the GB group (10 yr: 25 vs. 13%, respectively).


Figure 1
View larger version (17K):
[in this window]
[in a new window]
  		FIG. 1. Weight changes among subjects participating in the Swedish Obese Subjects study over a 10-yr period (11 ). There were 627 control subjects who did not undergo bariatric surgery, 156 who underwent banding, 451 who underwent vertical banded gastroplasty, and 34 who had gastric bypass.

 
In a two-cohort study by Christou et al. (21), percent excess weight loss decreased by about 25% from yr 2 to yr 16 (<20% follow-up) in patients who underwent RYGB or VBG surgeries. Weight change in the matched control group was not reported. The relative risk reduction in mortality in the bariatric surgery group was 89% during the 5-yr follow-up period. Compared with the controls, the bariatric surgery patients also had significantly lower relative risk for cancer, cardiovascular disease, hypertension, and type 2 diabetes during that period. The controls, other than being severely obese, were not closely matched to the patients by BMI.

Flum and Dellinger (23), in a retrospective cohort study from Washington, reported a modestly lower mortality rate in morbidly obese subjects who underwent RYGB surgery, compared with a nonoperated cohort of patients with morbid obesity at 15-yr follow-up. This study had a number of limitations. RYGB patients were significantly younger (43 vs. 47 yr, respectively) and more likely to be female (81 vs. 64%, respectively) than the controls. This may have partly accounted for the difference in mortality between the two groups. Factors such as race/ethnicity and degree of obesity, which affect mortality, were not reported. In addition, there was a substantial dropout rate in both the groups. Because this study was retrospective and the data were derived from the Hospital Abstract Reporting System and Vital Statistics databases, the information may be subject to errors. The authors also could not separate patients who underwent the open surgery vs. laparoscopy. The RYGB laparoscopic procedure is associated with lower incidence of incisional hernia than the open procedure (24).

In a retrospective cohort study, MacDonald et al. (22) compared morbidly obese type 2 diabetic patients who underwent RYGB surgery with type 2 diabetic controls who did not undergo surgery. The two groups were matched for age, weight, sex, BMI, and prevalence of hypertension. Percent excess weight loss was 62.4% at yr 1 and 50% at yr 14 in the surgery patients. Body weight of the matched patients with diabetes was not reported. The percent of diabetics requiring oral hypoglycemics or insulin decreased in the surgery group and increased in the control group. Mortality rate was lower in the surgery group than in the control group. The limitations of the study include a higher proportion of whites (76.6 vs. 50%, respectively) and a lower proportion of hypoglycemic medication use in patients undergoing surgery than in the controls (32 vs. 56%, respectively), which could have affected the results, retrospective cohort design, and limited sample size. In addition, information on the proportion of subjects who provided follow-up data were not provided.

Sugerman et al. (12) examined the database of patients who underwent RYGB surgery and reported a decrease in percent excess body weight loss from 66% at 1 yr (91% follow-up) to 52% at 10–12 yr (37% follow-up). Resolution of hypertension fell over that time, but resolution of diabetes was unchanged, although the value at yr 10–12 was not provided. These results are, however, difficult to interpret because of substantially different sample size at each follow-up and lack of a control group. Other uncontrolled case series studies (13, 14, 15, 16, 17, 19) have also reported a decrease in percent excess weight loss or percent weight loss over time after bariatric surgery but provided limited or no long-term data on comorbidities or major endpoints.

Two uncontrolled case series, on the other hand, reported successful long-term weight loss maintenance in RYGB (18) and GB (20) patients over 60 and 72 months, respectively. The validity of the results from these studies, however, may be questioned because the sample sizes decreased by more than 95% by the end of the studies.

In conclusion, RYGB and GB surgeries lead to substantial weight loss, but weight regain over the long term is not insignificant. According to the only well-designed, prospective, controlled study, the improvement in comorbidities seen initially mitigates in the long term possibly because of weight regain. There is also some evidence from a long-term retrospective study that RYGB surgery is associated with a modest reduction in mortality.


   Mechanisms for Weight Regain
Top
 Abstract
 Introduction
 Long-Term Effect of RYGB...
 Mechanisms for Weight Regain
Effect of Bariatric Surgery...
 Recommendations
 References
 
One possible mechanism for weight regain seen after 1 yr is increase in energy intake. Sjostrom et al. (11) reported daily intakes of about 2900, 1500, 1700, 1800, 1900, and 2000 kcal/d, respectively, at baseline and 6 months, 12 months, 2 yr, 3 yr, and 4–10 yr after surgery. The role of energy intake in weight regain may be greater than that observed because subjects tend to overadhere to their dietary recommendations on the day that the diet is assessed (25).

A possible reason for the increase in energy intake in RYGB patients may be due to dilatation of the gastric pouch and gastrojejunal anastomosis (26, 27). Late pouch dilatation has been reported in patients who undergo laparoscopic GB surgery (28) and is the leading indication for conversion of GB to a RYGB (29) but is seen less frequently after RYGB surgery (30). Revision surgery to correct these changes leads to improved weight loss (28, 29). However, these complications have been described in only a handful of patients, implying that other factors may be involved in modulating weight regain after bariatric surgery.

Regular physical activity is an important factor in weight loss maintenance (31). According to one survey in RYGB patients with a mean follow-up of 7 yr, successful patients (those who maintained at least 74% of their initial weight loss) exercised regularly (no details given) (32). In the prospective study by Sjostrom et al. (11), the approximate proportion of bariatric surgery patients who reported being active at work changed from 70% at baseline to 90% at yr 1 and 80% at yr 10. The proportion of patients who were active during leisure time was 55, 90, and 80%, respectively. The difference in the proportion active at work and during leisure time between the surgery patients and controls was narrower at 10 yr than at 1 yr. This may explain some of the observed weight regain seen in the surgery patients. Also physical activity may be overreported and thus needs to be assessed objectively. Whether increased physical activity in bariatric surgery patients is effective in weight loss maintenance remains to be proven by randomized trials.

Several studies have assessed metabolic rate in bariatric surgery patients (33, 34, 35, 36). van Gemert et al. (35) and Buscemi et al. (33) found a decrease in resting (33) or sleep (35) metabolic rate, even when expressed per kilogram fat-free mass, with weight loss in subjects who were followed up for 12 or 36–42 months, respectively, after surgery. Das et al. (36) and Flancbaum et al. (34), however, did not observe these changes at 14 and 24 months, respectively. Thus, the role of changes in energy expenditure in weight loss and maintenance needs to be studied more thoroughly.

The changes in energy intake, and perhaps even energy expenditure, seen after bariatric surgery may be affected by alterations in gut and adipocyte hormones. Gut hormones such as ghrelin, peptide YY (PYY), and glucagon-like-peptide (GLP)-1 have an important role in governing satiety (37). Of these, ghrelin is an orexigenic peptide, secreted primarily by the enteroendocrine cells in the fundus of stomach and acts through the hypothalamus (38, 39, 40, 41). Ghrelin levels have been found to increase after GB surgery (42, 43), although transiently in the case of one study (43), and suggest a role in weight regain after this procedure. Weight loss in RYGB surgery patients, however, is associated with a decrease in ghrelin levels, compared with weight loss after GB, biliopancreatic diversion, or conventional weight loss treatment (44, 45, 46, 47), and has often been considered to contribute to the marked efficacy of the RYGB, compared with the other procedures. This finding has, however, not been universally observed (48, 49). The conflicting data may be due to the different surgical techniques that affect the functional integrity of the gastric fundus from which ghrelin is mostly secreted. Whether the changes in ghrelin levels in bariatric surgery patients are maintained in the long term needs to be evaluated.

PYY secreted primarily by the more distal intestines in response to nutrient contact and GLP-1 secreted by the intestinal L cells induce satiety (50, 51, 52, 53). Clements et al. (54) reported no difference in fasting GLP-1 level 12 wk after RYGB surgery, compared with preoperative value. In weight-stable RYGB patients with an average follow-up of 35 months, fasting serum PYY level was similar to that of BMI-matched controls, but the PYY response to a test meal (320 kcal) was greater (55). Similarly Borg et al. (48) reported no change in fasting serum PYY and GLP-1 values but increased PYY and GLP-1 response to a test meal (420 kcal) at 6 months after RYGB surgery. The responses to a test meal suggest a beneficial effect on weight loss. It is possible that these changes gradually revert to presurgical levels and contribute to increased energy intake in the long term. Only long-term prospective studies can elucidate the influence of these hormones on energy balance.

According to a number of case series, serum leptin levels decreased with weight loss after bariatric surgery (56, 57, 58, 59, 60). The decrease was beyond the expected value based on body composition (57, 60). In a case-control study, serum leptin levels were lower in weight-stable RYGB patients 35 months after surgery, compared with BMI-matched controls (55). Given the putative adipostatic role of leptin, it is possible that relative hypoleptinemia may play a role in weight regain. Observational studies with very limited sample sizes, however, do not support the hypothesis that relative hypoleptinemia predicts weight regain in moderately obese or overweight subjects who lost modest amount of body weight (8–12 kg) (61, 62). Nevertheless, leptin administration in weight-stable subjects who lost weight via a liquid formula diet resulted in return of energy expenditure to preweight-loss levels (63). Information on energy intake was not reported (63).


   Effect of Bariatric Surgery on Nutritional Status and Intolerance
Top
 Abstract
 Introduction
 Long-Term Effect of RYGB...
 Mechanisms for Weight Regain
 Effect of Bariatric Surgery...
Recommendations
 References
 
Micronutrient deficiency

Deficiency of iron, vitamin B12, folate, calcium, and vitamin D has been frequently observed after RYGB surgery. Deficiency of vitamin A has also been observed, although less frequently. Nutrient deficiencies after GB surgery are less common because it does not have a malabsorptive component, and an adult multiple vitamin and mineral supplement is considered sufficient to prevent these problems (64). Reviewed below are the studies that have reported nutritional deficiencies in RYGB surgery patients (Table 2Go). The majority of these studies were uncontrolled case series, and so it is important to note that the studies may have somewhat overestimated the effect of surgery on nutritional status, especially given that nutritional deficiencies have been noted in severely obese subjects before surgery (65) and that many of the patients are menstruating women who are more likely to have poor iron status.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Effect of RYGB surgery on incidence of nutritional deficiencies

 
Serum iron deficiency is seen frequently in RYGB patients (66, 67, 68, 69), with the incidence rate as high as 52% (66). The incidence of anemia (type not specified) has been reported to be as high as 74% (66). Supplements containing usual daily doses of multivitamins (70), and even high doses of oral iron (320 mg twice daily) (71), do not consistently prevent anemia in menstruating women. Contributing factors to iron deficiency anemia include malabsorption due to bypassing of the duodenum and proximal jejunum, the main sites for iron absorption (Fig. 2Go); intolerance to iron-rich foods, especially red meat (15); and reduced stomach production of hydrochloric acid (72) required to reduce ferric iron to the ferrous state before it can be absorbed.


Figure 2
View larger version (31K):
[in this window]
[in a new window]
  		FIG. 2. Schematic representation of the normal gastrointestinal tract (A) and its perturbations in the two common bariatric surgery procedures, RYGB (B) and adjustable GB (C). A, Major sites of micronutrient absorption and gastrointestinal hormone production. Absorption of iron and other minerals such as calcium and magnesium occur mostly from the duodenum and proximal jejunum. Whereas the absorption of dietary fats and concomitantly the fat-soluble vitamins such as vitamins A and D occurs in the distal small intestine, it is facilitated by the action of pancreatic enzymes and bile salts released into the duodenum. Water-soluble vitamins are absorbed throughout the small intestine. Among the gastrointestinal hormones, ghrelin is secreted predominantly from the gastric fundus. Glucose-dependent insulinotropic peptide (GIP) and cholecystokinin (CCK) are secreted mostly from the proximal small intestine, whereas the distal intestines are the primary site of production of the satiety-inducing hormones, GLP-1 and PYY. B, In RYGB, the stomach is divided into a small proximal pouch, excluding much of the ghrelin-secreting regions, and a larger distal segment. The pouch is anastomosed with the proximal jejunum through a narrow end to side anastomosis, whereas the distal segment along with the duodenum and part of the jejunum are attached to the distal jejunum. This surgery combines restrictive and malabsorptive procedures. C, GB is a purely restrictive procedure in which the prosthetic band divides the stomach into a small proximal segment and a larger distal segment. The band aperture between the two segments can be adjusted by changing the volume of the saline reservoir, which has a sc port.

 
Vitamin B12 deficiency, assessed by serum vitamin B12 levels, is also frequently seen in RYGB patients (66, 67, 68, 69, 73) with the incidence rate as high as 64% (67). Most vitamin B12 deficiencies in RYGB patients may be corrected by 500 µg/d oral B12 supplementation (74), and a minimum dose of 300 µg crystalline B12 per day is necessary to maintain normal serum levels (75). Only a small number of patients require parenteral administration of B12 (2000 µg/month) (64). Possible factors that contribute to B12 deficiency include achlorhydria (72), which prevents its cleavage from foods; decreased consumption due to intolerance to its main sources (milk and meat) (15); and poor secretion of intrinsic factor needed for its absorption (73). Because of the latter problem, Elliot (64) recommended taking the supplement in a sublingual form.

Serum folate deficiency has been reported to be as high 38% after RYGB surgery (67). Brolin et al. (74) reported that a supplement containing 400 µg of folate per day consistently corrected low folate levels in patients who underwent RYGB surgery, although 1000 µg/d have been recommended by others (64). Primary reason for folate deficiency is decreased folate intake. Malabsorption may not play a big role, even though folate is preferentially absorbed in the proximal part of the small intestine, because absorption can occur along the entire part of the small intestine with adaptation after surgery (76). Maintaining adequate folate levels is important, however, because of the possibility of megaloblastic anemia. Also, there have been reports of neural tube defects in infants born to mothers who underwent RYGB surgery (77, 78).

Calcium and vitamin D deficiency may occur in patients who undergo RYGB surgery, and a deficiency rate of 10% for serum calcium and 51% for serum 25-hydroxy vitamin D levels has been reported (66). PTH levels, however, were not reported (66). Possible contributors to calcium deficiency in the RYGB patients include malabsorption of calcium because of bypassing the duodenum and proximal jejunum in which calcium is mostly absorbed; intolerance to rich sources of calcium such as milk; and defective absorption of vitamin D because of fat malabsorption. Fat malabsorption is due to the short common channel and delayed mixing of fat with pancreatic enzymes and bile salts as a result of bypassing the duodenum. Deficiency of calcium is not always apparent, however, because of release of calcium from bone. Coates et al. (79) and von Mach et al. (80), who followed subjects for 9 and 24 months, respectively, reported elevated markers of bone turnover and/or decreased bone mass in patients who underwent RYGB surgery, compared with patients who underwent GB surgery (80) or the matched obese controls (79, 80). The higher bone turnover in the RYGB patients, however, may be partly due to the increased weight loss in these patients, compared with the other patients. PTH levels were not different between the RYGB and obese control groups (80) nor did they change over time after surgery (79). Nevertheless, to prevent metabolic bone disease, 1200–1500 mg/d of calcium and 400 IU/d of vitamin D supplements are recommended (64, 65). These amounts, however, may not suppress serum PTH or bone resorption, and increased supplementation may need to be considered (81). Because of reduced stomach acid content, calcium citrate rather than calcium carbonate is recommended because the latter requires acid for absorption (64, 65). Regular monitoring of markers of bone resorption such as urinary N-telopeptide level and markers of bone formation such as serum osteocalcin level may also be necessary.

Serum vitamin A deficiency has been reported in 10% of RYGB patients (66, 67). Whereas symptoms of vitamin A deficiency are rare in this population, a case study reported xerophthalmia and nyctalopia in a patient after a duodenal switch gastric bypass surgery due to inadequate vitamin A supplementation (82). A contributing factor to vitamin A deficiency in RYGB patients is fat malabsorption. Careful monitoring of serum vitamin A status and supplementation as needed is necessary to avoid a deficiency.

Despite the evidence of nutritional deficiencies, many surgeons do not recommend adequate supplements or evaluate serum nutrient levels (83), and most patients do not comply with the recommended supplement regimen (70). Education of both the physicians and patients is thus necessary to prevent malnutrition after RYGB surgery.

Macronutrient deficiency and intolerance

Protein deficiency, assessed by serum albumin levels, is less common than most other nutrient deficiencies (Table 2Go) (66, 67, 68, 69). To consume enough protein, patients should be advised to consume fish, which is better tolerated than meat.

Simple sugar intake, especially added sugars (64), has been reported to cause dumping syndrome in as many as 76% (84) of the RYGB patients. The food rapidly enters the small intestine causing an osmotic load, which leads to movement of fluid from the blood into the intestine (85, 86). Rapid food entry into the jejunum also stimulates a substantial release of peptide hormones (85, 86). Clinical manifestations of the dumping syndrome include gastrointestinal symptoms such as early satiety, nausea, cramps, and explosive diarrhea and vasomotor symptoms such as sweating, flushing, palpitations, dizziness, and an intense desire to lie down (85). The insulin response is exaggerated and causes hypoglycemia (85, 86). To prevent dumping syndrome, patients should avoid consuming fruit juices and foods and drinks with added sugar (64); consume frequent, small, dry meals because water can make the food more soluble; include dietary fiber; increase dietary protein (especially fish and chicken); and modestly increase dietary fat (to delay gastric emptying) (86).


   Recommendations
Top
 Abstract
 Introduction
 Long-Term Effect of RYGB...
 Mechanisms for Weight Regain
 Effect of Bariatric Surgery...
 Recommendations
References
 
It is often stated that bariatric surgery is the most effective way of treating morbid obesity. Yet this conclusion has been based on largely uncontrolled case series. Randomized, controlled studies comparing morbidly obese subjects who undergo either bariatric surgery or conventional treatment have not been conducted for the following reasons: many surgeons believe that conventional therapy is inferior to surgery, and therefore it may be unethical to randomize; and patients may not be willing to be randomized to a nonsurgical group because they believe they have already tried all the conventional approaches to lose weight. Despite the difficulty of randomizing subjects, it is imperative that the effect of bariatric surgery vs. traditional weight loss strategies on long-term outcomes such as weight maintenance, comorbidities, and mortality be compared by well-designed, long-term (at least 5 yr), randomized, controlled studies.

Other weaknesses of many bariatric surgery studies include a lack of information on sample size at each follow-up and a nonstandardized way of presenting data on weight loss. Data analysis should be conducted on subjects with a complete set of data as well as the entire group with missing data replaced by baseline data. To facilitate comparison of weight loss across studies, all studies should provide information on body weight and BMI at each time point. Patient characteristics such as gender, age, socioeconomic status, fat distribution, race/ethnicity, etc. that may determine weight change need to be reported.

The role of energy intake and expenditure, physical activity, gut and adipocyte hormones, and stoma changes in weight regain need to be further elucidated by long-term prospective studies. Effect of exercise on weight loss maintenance in bariatric surgery patients needs to be evaluated by randomized, controlled studies.

Because nutritional deficiencies are common in RYGB patients, aggressive supplementation with iron, vitamin B12, folate, calcium, and vitamin D and regular monitoring of nutrition status are necessary. Careful screening before surgery may help to select patients who are more likely to be compliant to supplement recommendations. Women of child-bearing age should be counseled to avoid getting pregnant while actively losing weight and until the serum nutrient levels are normalized. To prevent dumping syndrome, patients should be encouraged to consume frequent, small meals, avoiding fruit juices and added sugars.

In conclusion, bariatric surgeries have a place in treatment of carefully selected patients with morbid obesity. These patients should be encouraged to increase physical activity to possibly prevent weight regain over the long term and consume vitamin and mineral supplements to prevent nutritional deficiencies.


   Acknowledgments
 
The authors thank Meredith Millay and Robert Butsch for illustrations and Patty Ashworth for secretarial assistance.


   Footnotes
 
Disclosure statement: The authors have nothing to declare.

First Published Online September 5, 2006

Abbreviations: BMI, Body mass index; GB, gastric banding; GLP, glucagon-like-peptide; HDL, high-density lipoprotein; PYY, peptide YY; RYGB, Roux-en-Y gastric bypass; VBG, vertical banded gastroplasty.

Received March 13, 2006.

Accepted August 28, 2006.


   References
Top
 Abstract
 Introduction
 Long-Term Effect of RYGB...
 Mechanisms for Weight Regain
 Effect of Bariatric Surgery...
 Recommendations
 References
 

  1. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM 2006 Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 295:1549–1555[Abstract/Free Full Text]
  2. Sturm R 2003 Increases in clinically severe obesity in the United States, 1986–2000. Arch Intern Med 163:2146–2148[Abstract/Free Full Text]
  3. Must A, Spadano J, Coakley EH, Field AE, Colditz G, Dietz WH 1999 The disease burden associated with overweight and obesity. JAMA 282:1523–1529[Abstract/Free Full Text]
  4. 2000 Overweight, obesity, and health risk. National Task Force on the Prevention and Treatment of Obesity. Arch Intern Med 160:898–904
  5. Fontaine KR, Redden DT, Wang C, Westfall AO, Allison DB 2003 Years of life lost due to obesity. JAMA 289:187–193[Abstract/Free Full Text]
  6. 1998 Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults–the evidence report. National Institutes of Health. Obes Res 6(Suppl 2):51S–209S
  7. North American Association for the Study of Obesity and the National Heart, Lung, and Blood Institute 2000 The practical guide: identification, evaluation, and treatment of overweight and obesity in adults. NIH publication 00-4084
  8. Santry HP, Gillen DL, Lauderdale DS 2005 Trends in bariatric surgical procedures. JAMA 294:1909–1917[Abstract/Free Full Text]
  9. Steinbrook R 2004 Surgery for severe obesity. N Engl J Med 350:1075–1079[Free Full Text]
  10. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K 2004 Bariatric surgery: a systematic review and meta-analysis. JAMA 292:1724–1737[Abstract/Free Full Text]
  11. Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, Dahlgren S, Larsson B, Narbro K, Sjostrom CD, Sullivan M, Wedel H 2004 Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 351:2683–2693[Abstract/Free Full Text]
  12. Sugerman HJ, Wolfe LG, Sica DA, Clore JN 2003 Diabetes and hypertension in severe obesity and effects of gastric bypass-induced weight loss. Ann Surg 237:751–756; discussion 757–758[CrossRef][Medline]
  13. Waters GS, Pories WJ, Swanson MS, Meelheim HD, Flickinger EG, May HJ 1991 Long-term studies of mental health after the Greenville gastric bypass operation for morbid obesity. Am J Surg 161:154–157; discussion 157–158[CrossRef][Medline]
  14. van de Weijgert EJ, Ruseler CH, Elte JW 1999 Long-term follow-up after gastric surgery for morbid obesity: preoperative weight loss improves the long-term control of morbid obesity after vertical banded gastroplasty. Obes Surg 9:426–432[CrossRef][Medline]
  15. Balsiger BM, Kennedy FP, Abu-Lebdeh HS, Collazo-Clavell M, Jensen MD, O’Brien T, Hensrud DD, Dinneen SF, Thompson GB, Que FG, Williams DE, Clark MM, Grant JE, Frick MS, Mueller RA, Mai JL, Sarr MG 2000 Prospective evaluation of Roux-en-Y gastric bypass as primary operation for medically complicated obesity. Mayo Clin Proc 75:673–680[Abstract]
  16. Yale CE 1989 Gastric surgery for morbid obesity. Complications and long-term weight control. Arch Surg 124:941–946[Abstract/Free Full Text]
  17. Martikainen T, Pirinen E, Alhava E, Poikolainen E, Paakkonen M, Uusitupa M, Gylling H 2004 Long-term results, late complications and quality of life in a series of adjustable gastric banding. Obes Surg 14:648–654[CrossRef][Medline]
  18. Wittgrove AC, Clark GW 2000 Laparoscopic gastric bypass, Roux-en-Y-500 patients: technique and results, with 3–60 month follow-up. Obes Surg 10:233–239[CrossRef][Medline]
  19. Pories WJ, Swanson MS, MacDonald KG, Long SB, Morris PG, Brown BM, Barakat HA, deRamon RA, Israel G, Dolezal JM 1995 Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg 222:339–350; discussion 350–352[Medline]
  20. O’Brien PE, Dixon JB, Brown W, Schachter LM, Chapman L, Burn AJ, Dixon ME, Scheinkestel C, Halket C, Sutherland LJ, Korin A, Baquie P 2002 The laparoscopic adjustable gastric band (Lap-Band): a prospective study of medium-term effects on weight, health and quality of life. Obes Surg 12:652–660[CrossRef][Medline]
  21. Christou NV, Sampalis JS, Liberman M, Look D, Auger S, McLean AP, MacLean LD 2004 Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients. Ann Surg 240:416–423; discussion 423–424[Medline]
  22. MacDonald Jr KG, Long SD, Swanson MS, Brown BM, Morris P, Dohm GL, Pories WJ 1997 The gastric bypass operation reduces the progression and mortality of non-insulin-dependent diabetes mellitus. J Gastrointest Surg 1:213–220[CrossRef][Medline]
  23. Flum DR, Dellinger EP 2004 Impact of gastric bypass operation on survival: a population-based analysis. J Am Coll Surg 199:543–551[CrossRef][Medline]
  24. Puzziferri N, Austrheim-Smith IT, Wolfe BM, Wilson SE, Nguyen NT 2006 Three-year follow-up of a prospective randomized trial comparing laparoscopic versus open gastric bypass. Ann Surg 243:181–188[CrossRef][Medline]
  25. Forster JL, Jeffery RW, VanNatta M, Pirie P 1990 Hypertension prevention trial: do 24-h food records capture usual eating behavior in a dietary change study? Am J Clin Nutr 51:253–257[Abstract/Free Full Text]
  26. Schwartz RW, Strodel WE, Simpson WS, Griffen Jr WO 1988 Gastric bypass revision: lessons learned from 920 cases. Surgery 104:806–812[Medline]
  27. Muller MK, Wildi S, Scholz T, Clavien PA, Weber M 2005 Laparoscopic pouch resizing and redo of gastro-jejunal anastomosis for pouch dilatation following gastric bypass. Obes Surg 15:1089–1095[CrossRef][Medline]
  28. Niville E, Dams A 1999 Late pouch dilation after laparoscopic adjustable gastric and esophagogastric banding: incidence, treatment, and outcome. Obes Surg 9:381–384[CrossRef][Medline]
  29. Mognol P, Chosidow D, Marmuse JP 2004 Laparoscopic conversion of laparoscopic gastric banding to Roux-en-Y gastric bypass: a review of 70 patients. Obes Surg 14:1349–1353[CrossRef][Medline]
  30. Weber M, Muller MK, Bucher T, Wildi S, Dindo D, Horber F, Hauser R, Clavien PA 2004 Laparoscopic gastric bypass is superior to laparoscopic gastric banding for treatment of morbid obesity. Ann Surg 240:975–982; discussion 982–983[CrossRef][Medline]
  31. Wing RR, Hill JO 2001 Successful weight loss maintenance. Annu Rev Nutr 21:323–341[CrossRef][Medline]
  32. Cook CM, Edwards C 1999 Success habits of long-term gastric bypass patients. Obes Surg 9:80–82[CrossRef][Medline]
  33. Buscemi S, Caimi G, Verga S 1996 Resting metabolic rate and postabsorptive substrate oxidation in morbidly obese subjects before and after massive weight loss. Int J Obes Relat Metab Disord 20:41–46[Medline]
  34. Flancbaum L, Choban PS, Bradley LR, Burge JC 1997 Changes in measured resting energy expenditure after Roux-en-Y gastric bypass for clinically severe obesity. Surgery 122:943–949[CrossRef][Medline]
  35. van Gemert WG, Westerterp KR, van Acker BA, Wagenmakers AJ, Halliday D, Greve JM, Soeters PB 2000 Energy, substrate and protein metabolism in morbid obesity before, during and after massive weight loss. Int J Obes Relat Metab Disord 24:711–718[CrossRef][Medline]
  36. Das SK, Roberts SB, McCrory MA, Hsu LK, Shikora SA, Kehayias JJ, Dallal GE, Saltzman E 2003 Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. Am J Clin Nutr 78:22–30[Abstract/Free Full Text]
  37. Murphy KG, Bloom SR 2004 Gut hormones in the control of appetite. Exp Physiol 89:507–516[Abstract/Free Full Text]
  38. Tschop M, Smiley DL, Heiman ML 2000 Ghrelin induces adiposity in rodents. Nature 407:908–913[CrossRef][Medline]
  39. Date Y, Kojima M, Hosoda H, Sawaguchi A, Mondal MS, Suganuma T, Matsukura S, Kangawa K, Nakazato M 2000 Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141:4255–4261[Abstract/Free Full Text]
  40. Ariyasu H, Takaya K, Tagami T, Ogawa Y, Hosoda K, Akamizu T, Suda M, Koh T, Natsui K, Toyooka S, Shirakami G, Usui T, Shimatsu A, Doi K, Hosoda H, Kojima M, Kangawa K, Nakao K 2001 Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab 86:4753–4758[Abstract/Free Full Text]
  41. Wren AM, Seal LJ, Cohen MA, Brynes AE, Frost GS, Murphy KG, Dhillo WS, Ghatei MA, Bloom SR 2001 Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab 86:5992
  42. Hanusch-Enserer U, Cauza E, Brabant G, Dunky A, Rosen H, Pacini G, Tuchler H, Prager R, Roden M 2004 Plasma ghrelin in obesity before and after weight loss after laparoscopical adjustable gastric banding. J Clin Endocrinol Metab 89:3352–3358[Abstract/Free Full Text]
  43. Mariani LM, Fusco A, Turriziani M, Veneziani A, Marini MA, de Lorenzo A, Bertoli A 2005 Transient increase of plasma ghrelin after laparoscopic adjustable gastric banding in morbid obesity. Horm Metab Res 37:242–245[CrossRef][Medline]
  44. Cummings DE, Weigle DS, Frayo RS, Breen PA, Ma MK, Dellinger EP, Purnell JQ 2002 Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 346:1623–1630[Abstract/Free Full Text]
  45. Fruhbeck G, Diez-Caballero A, Gil MJ, Montero I, Gomez-Ambrosi J, Salvador J, Cienfuegos JA 2004 The decrease in plasma ghrelin concentrations following bariatric surgery depends on the functional integrity of the fundus. Obes Surg 14:606–612[CrossRef][Medline]
  46. Fruhbeck G, Rotellar F, Hernandez-Lizoain JL, Gil MJ, Gomez-Ambrosi J, Salvador J, Cienfuegos JA 2004 Fasting plasma ghrelin concentrations 6 months after gastric bypass are not determined by weight loss or changes in insulinemia. Obes Surg 14:1208–1215[CrossRef][Medline]
  47. Cummings DE, Overduin J, Foster-Schubert KE 2004 Gastric bypass for obesity: mechanisms of weight loss and diabetes resolution. J Clin Endocrinol Metab 89:2608–2615[Free Full Text]
  48. Borg CM, le Roux CW, Ghatei MA, Bloom SR, Patel AG, Aylwin SJ 2006 Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Br J Surg 93:210–215[CrossRef][Medline]
  49. Holdstock C, Engstrom BE, Ohrvall M, Lind L, Sundbom M, Karlsson FA 2004 Effect of bariatric surgery on adipose tissue regulatory peptides and growth hormone secretion. Asia Pac J Clin Nutr 13:S41
  50. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, Ghatei MA, Bloom SR 2003 Inhibition of food intake in obese subjects by peptide YY3–36. N Engl J Med 349:941–948[Abstract/Free Full Text]
  51. Dube PE, Brubaker PL 2004 Nutrient, neural and endocrine control of glucagon-like peptide secretion. Horm Metab Res 36:755–760[CrossRef][Medline]
  52. D’Alessio DA, Vahl TP 2004 Glucagon-like peptide 1: evolution of an incretin into a treatment for diabetes. Am J Physiol Endocrinol Metab 286:E882–E890
  53. Brubaker PL, Drucker DJ 2004 Minireview: glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology 145:2653–2659[CrossRef][Medline]
  54. Clements RH, Gonzalez QH, Long CI, Wittert G, Laws HL 2004 Hormonal changes after Roux-en Y gastric bypass for morbid obesity and the control of type-II diabetes mellitus. Am Surg 70:1–4; discussion 4–5[Medline]
  55. Korner J, Bessler M, Cirilo LJ, Conwell IM, Daud A, Restuccia NL, Wardlaw SL 2005 Effects of Roux-en-Y gastric bypass surgery on fasting and postprandial concentrations of plasma ghrelin, peptide YY, and insulin. J Clin Endocrinol Metab 90:359–365[Abstract/Free Full Text]
  56. Molina A, Vendrell J, Gutierrez C, Simon I, Masdevall C, Soler J, Gomez JM 2003 Insulin resistance, leptin and TNF-{alpha} system in morbidly obese women after gastric bypass. Obes Surg 13:615–621[CrossRef][Medline]
  57. Infanger D, Baldinger R, Branson R, Barbier T, Steffen R, Horber FF 2003 Effect of significant intermediate-term weight loss on serum leptin levels and body composition in severely obese subjects. Obes Surg 13:879–888[CrossRef][Medline]
  58. Nijhuis J, van Dielen FM, Buurman WA, Greve JW 2004 Ghrelin, leptin and insulin levels after restrictive surgery: a 2-year follow-up study. Obes Surg 14:783–787[CrossRef][Medline]
  59. Uzun H, Zengin K, Taskin M, Aydin S, Simsek G, Dariyerli N 2004 Changes in leptin, plasminogen activator factor and oxidative stress in morbidly obese patients following open and laparoscopic Swedish adjustable gastric banding. Obes Surg 14:659–665[CrossRef][Medline]
  60. Coupaye M, Bouillot JL, Coussieu C, Guy-Grand B, Basdevant A, Oppert JM 2005 One-year changes in energy expenditure and serum leptin following adjustable gastric banding in obese women. Obes Surg 15:827–833[CrossRef][Medline]
  61. Nagy TR, Davies SL, Hunter GR, Darnell B, Weinsier RL 1998 Serum leptin concentrations and weight gain in postobese, postmenopausal women. Obes Res 6:257–261[Medline]
  62. Wing RR, Sinha MK, Considine RV, Lang W, Cargo JF 1996 Relationship between weight loss maintenance and changes in serum leptin levels. Horm Metab Res 28:698–703[Medline]
  63. Rosenbaum M, Goldsmith R, Bloomfield D, Magnano A, Weimer L, Heymsfield S, Gallagher D, Mayer L, Murphy E, Leibel RL 2005 Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J Clin Invest 115:3579–3586[CrossRef][Medline]
  64. Elliot K 2003 Nutritional considerations after bariatric surgery. Crit Care Nurs Q 26:133–138[Medline]
  65. Bloomberg RD, Fleishman A, Nalle JE, Herron DM, Kini S 2005 Nutritional deficiencies following bariatric surgery: what have we learned? Obes Surg 15:145–154[CrossRef][Medline]
  66. Brolin RE, LaMarca LB, Kenler HA, Cody RP 2002 Malabsorptive gastric bypass in patients with superobesity. J Gastrointest Surg 6:195–203; discussion 204–205[CrossRef][Medline]
  67. Halverson JD 1986 Micronutrient deficiencies after gastric bypass for morbid obesity. Am Surg 52:594–598[Medline]
  68. Kalfarentzos F, Dimakopoulos A, Kehagias I, Loukidi A, Mead N 1999 Vertical banded gastroplasty versus standard or distal Roux-en-Y gastric bypass based on specific selection criteria in the morbidly obese: preliminary results. Obes Surg 9:433–442[CrossRef][Medline]
  69. Skroubis G, Sakellaropoulos G, Pouggouras K, Mead N, Nikiforidis G, Kalfarentzos F 2002 Comparison of nutritional deficiencies after Roux-en-Y gastric bypass and after biliopancreatic diversion with Roux-en-Y gastric bypass. Obes Surg 12:551–558[CrossRef][Medline]
  70. Brolin RE, Gorman RC, Milgrim LM, Kenler HA 1991 Multivitamin prophylaxis in prevention of post-gastric bypass vitamin and mineral deficiencies. Int J Obes 15:661–667[Medline]
  71. Brolin RE, Gorman JH, Gorman RC, Petschenik AJ, Bradley LB, Kenler HA, Cody RP 1998 Prophylactic iron supplementation after Roux-en-Y gastric bypass: a prospective, double-blind, randomized study. Arch Surg 133:740–744[Abstract/Free Full Text]
  72. Smith CD, Herkes SB, Behrns KE, Fairbanks VF, Kelly KA, Sarr MG 1993 Gastric acid secretion and vitamin B12 absorption after vertical Roux-en-Y gastric bypass for morbid obesity. Ann Surg 218:91–96[Medline]
  73. Marcuard SP, Sinar DR, Swanson MS, Silverman JF, Levine JS 1989 Absence of luminal intrinsic factor after gastric bypass surgery for morbid obesity. Dig Dis Sci 34:1238–1242[CrossRef][Medline]
  74. Brolin RE, Gorman JH, Gorman RC, Petschenik AJ, Bradley LJ, Kenler HA, Cody RP 1998 Are vitamin B12 and folate deficiency clinically important after Roux-en-Y gastric bypass? J Gastrointest Surg 2:436–442[CrossRef][Medline]
  75. Rhode BM, Arseneau P, Cooper BA, Katz M, Gilfix BM, MacLean LD 1996 Vitamin B-12 deficiency after gastric surgery for obesity. Am J Clin Nutr 63:103–109[Abstract/Free Full Text]
  76. Alvarez-Leite JI 2004 Nutrient deficiencies secondary to bariatric surgery. Curr Opin Clin Nutr Metab Care 7:569–575[CrossRef][Medline]
  77. Martin L, Chavez GF, Adams Jr MJ, Mason EE, Hanson JW, Haddow JE, Currier RW 1988 Gastric bypass surgery as maternal risk factor for neural tube defects. Lancet 1:640–641[Medline]
  78. Knudsen LB, Kallen B 1986 Gastric bypass, pregnancy, and neural tube defects. Lancet 2:227
  79. Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL 2004 Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab 89:1061–1065[Abstract/Free Full Text]
  80. von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U 2004 Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism 53:918–921[CrossRef][Medline]
  81. Goode LR, Brolin RE, Chowdhury HA, Shapses SA 2004 Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res 12:40–47[Medline]
  82. Lee WB, Hamilton SM, Harris JP, Schwab IR 2005 Ocular complications of hypovitaminosis a after bariatric surgery. Ophthalmology 112:1031–1034[CrossRef][Medline]
  83. Brolin RE, Leung M 1999 Survey of vitamin and mineral supplementation after gastric bypass and biliopancreatic diversion for morbid obesity. Obes Surg 9:150–154[CrossRef][Medline]
  84. Mallory GN, Macgregor AM, Rand CS 1996 The influence of dumping on weight loss after gastric restrictive surgery for morbid obesity. Obes Surg 6:474–478[CrossRef][Medline]
  85. Ukleja A 2005 Dumping syndrome: pathophysiology and treatment. Nutr Clin Pract 20:517–525[Abstract/Free Full Text]
  86. Stocker DJ 2003 Management of the bariatric surgery patient. Endocrinol Metab Clin North Am 32:437–457[CrossRef][Medline]



This article has been cited by other articles:


Home page
 Am. J. Clin. Nutr.Home page
M. Ruz, F. Carrasco, P. Rojas, J. Codoceo, J. Inostroza, A. Rebolledo, K. Basfi-fer, A. Csendes, K. Papapietro, F. Pizarro, et al.
Iron absorption and iron status are reduced after Roux-en-Y gastric bypass
Am. J. Clinical Nutrition, September 1, 2009; 90(3): 527 - 532.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
S. Savastano, C. Di Somma, L. Angrisani, F. Orio, S. Longobardi, G. Lombardi, and A. Colao
Growth Hormone Treatment Prevents Loss of Lean Mass after Bariatric Surgery in Morbidly Obese Patients: Results of a Pilot, Open, Prospective, Randomized, Controlled Study
J. Clin. Endocrinol. Metab., March 1, 2009; 94(3): 817 - 826.
[Abstract] [Full Text] [PDF]

Home page
 ANN INTERN MEDHome page
M. L. Vetter, S. Cardillo, M. R. Rickels, and N. Iqbal
Narrative Review: Effect of Bariatric Surgery on Type 2 Diabetes Mellitus
Ann Intern Med, January 20, 2009; 150(2): 94 - 103.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
A. V. Mayorov, N. Amara, J. Y. Chang, J. A. Moss, M. S. Hixon, D. I. Ruiz, M. M. Meijler, E. P. Zorrilla, and K. D. Janda
Catalytic antibody degradation of ghrelin increases whole-body metabolic rate and reduces refeeding in fasting mice
PNAS, November 11, 2008; 105(45): 17487 - 17492.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
J. Fleischer, E. M. Stein, M. Bessler, M. D. Badia, N. Restuccia, L. Olivero-Rivera, D. J. McMahon, and S. J. Silverberg
The Decline in Hip Bone Density after Gastric Bypass Surgery Is Associated with Extent of Weight Loss
J. Clin. Endocrinol. Metab., October 1, 2008; 93(10): 3735 - 3740.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
M. Riedl, G. Vila, C. Maier, A. Handisurya, S. Shakeri-Manesch, G. Prager, O. Wagner, A. Kautzky-Willer, B. Ludvik, M. Clodi, et al.
Plasma Osteopontin Increases After Bariatric Surgery and Correlates with Markers of Bone Turnover But Not with Insulin Resistance
J. Clin. Endocrinol. Metab., June 1, 2008; 93(6): 2307 - 2312.
[Abstract] [Full Text] [PDF]

Home page
 Arch. Dis. Child.Home page
J P H Shield, E Crowne, and J Morgan
Is there a place for bariatric surgery in treating childhood obesity?
Arch. Dis. Child., May 1, 2008; 93(5): 369 - 372.
[Full Text] [PDF]

Home page
 Nutr Clin PractHome page
S. F. Clark
Iron Deficiency Anemia
Nutr Clin Pract, April 1, 2008; 23(2): 128 - 141.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shah, M.
Right arrow Articles by Garg, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shah, M.
Right arrow Articles by Garg, A.
Related Collections
Right arrow Metabolism
Right arrow Obesity

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals