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Table of Contents   
REVIEW ARTICLE  
Year : 2015  |  Volume : 21  |  Issue : 5  |  Page : 269-277
Endocrine and metabolic complications after bariatric surgery


Department of Medicine, King Saud University, Riyadh, Kingdom of Saudi Arabia

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Date of Submission22-Feb-2015
Date of Acceptance25-Feb-2015
Date of Web Publication29-Sep-2015
 

   Abstract 

Bariatric surgery is the most effective therapeutic option for obese patients; however, it carries substantial risks, including procedure-related complications, malabsorption, and hormonal disturbance. Recent years have seen an increase in the bariatric surgeries performed utilizing either an independent or a combination of restrictive and malabsorptive procedures. We review some complications of bariatric procedures more specifically, hypoglycemia and osteoporosis, the recommended preoperative assessment and then regular follow up, and the therapeutic options. Surgeon, internist, and the patient must be aware of the multiple risks of this kind of surgery and the needed assessment and follow up.

Keywords: Bariatric surgery, beta cell mass, dual energy X-ray absorptiometry, glucagon-like peptides, hypoglycemia, nesidioblastosis, osteoporosis

How to cite this article:
Jammah AA. Endocrine and metabolic complications after bariatric surgery. Saudi J Gastroenterol 2015;21:269-77

How to cite this URL:
Jammah AA. Endocrine and metabolic complications after bariatric surgery. Saudi J Gastroenterol [serial online] 2015 [cited 2019 Dec 14];21:269-77. Available from: http://www.saudijgastro.com/text.asp?2015/21/5/269/164183


The increase in the prevalence of overweight and obesity in recent years has seen an unprecedented rise so much so that they are now considered to have reached epidemic proportions in many parts of the world. The World Health Organization (WHO) projections [1] indicate that, by 2015, 2.3 billion adults will be overweight and 700 million will be obese.

In the United States alone, as per the National Health and Nutrition Examination Survey 2009–2010, about one third of US population approximately equal to 130 million adults [2] are obese. In Saudi Arabia itself the extent of the problem based on 2005 surveillance reported prevalence rates for overweight and obesity to be approximately 42.4% and 36%, respectively.[3]The body mass index (BMI) is a simple and effective method to define levels of obesity. The healthy weight ranges from 18.5 to 24.9 kg/m 2, overweight from 25 to 30 kg/m 2, whereas obesity is defined as BMI ≥30 kg/m 2 and classified into groups:[4]

  • Class 1, BMI from 30 to 34.9 kg/m 2
  • Class 2, BMI from 35 to 39.9 kg/m 2
  • Class 3 (severe obesity), BMI ≥40 kg/m 2
  • Class 4 (super obesity), BMI from 50 to 59.9 kg/m 2.


Obesity is a major health concern by itself and is associated with many fatal and nonfatal chronic conditions such as hypertension, hyperinsulinemia, diabetes mellitus, hypertriglyceridemia, low serum high-density lipoprotein (HDL) cholesterol concentration, hypercholesterolemia,[5] heart disease, hyperurecemia, gallstones, cancers, and stroke.[6] These obesity - associated comorbid conditions increase greatly with BMI >30 kg/m 2, increasing the risk of morbidity and mortality significantly and are estimated to increase the risk for premature death from all causes by 50%–100%.[7],[8] The expected life span of a Caucasian male with a BMI >30 kg/m 2 is reduced by 9 years,[9] whereas that of individuals of BMI > 45 kg/m 2 is associated with a decrease of 13 years of life expectancy compared with a lean individuals (20–22 kg/m 2).[10] Although the increase in the number of cases of obese has levelled off, a marked increase in the number of cases with morbid obesity has been observed in recent years.[11]

The mainstay of treatment for obesity has been either medically through lifestyle modifications, dietary interventions, and pharmacotherapy or surgically through bariatric surgery. The poor short- and long-term outcomes of the presently applied medical modalities of treatment furthered the number of bariatric procedures. Bariatric surgery has become the most successful treatment for obesity in individuals who have failed at supervised medical weight loss, which achieves a significant and durable weight loss. The incidence of diabetes in the obese has been noted in many studies to have either reduced after surgery or become completely resolved in 77% of cases. The incidence of hyperlipidemia improved in 70% or more of patients, hypertension in 62%, and obstructive sleep apnea resolved in 86%. Gastroesophageal reflux symptoms demonstrated improvements with a complete or partial regression of Barrett's esophagus, and urinary stress incontinence episodes decreased by 47% in women who achieved 8% weight loss.[12],[13] These figures roughly translate into a 29% reduction of obesity-related morbidity and mortality following surgery. In another cohort, deaths from all causes were reduced by 40%, from diabetes by 92%, from coronary disease by 56%, and from cancers by 60%.[14],[15],[16] The beneficial effect of the common bariatric procedures has been shown to occur via increased glucose and lipid metabolism and due to alterations in hormonal mechanisms controlling the body's hunger and satiety responses subsequently leading to an overall change in metabolism. Based on these findings, there has been a paradigm shift in the concept and aim of performing the bariatric surgery from interventions primarily directed to obesity, to the broader category of treating metabolic disorders, for example, type2 diabetes. This has raised the possibility that these procedures should be considered "metabolic," instead of surgeries intended for just weight reduction.[17] Recent years have seen an increase in laparoscopically performed bariatric surgery utilizing either an independent or a combination of restrictive and malabsorptive procedures. The optimal choice for the type of bariatric procedure depends on many factors that include goals of therapy, available local–regional expertise (surgeon and institution), patient preferences, and preoperative risk stratification.[18] Routinely employed techniques include (1) adjustable gastric band (LAGB), (2) biliopancreatic diversion (BPD) with duodenal switch (BPDDS), (3) sleeve gastrectomy (LSG), and (4) Roux-en-Y gastric bypass (RYGB).[19],[20],[21],[22],[23] The loss of initial body weight and the equivalent excess body weight loss differ with the type of procedure. Gastric banding results in an average loss of 20%–30% of initial body weight [24] equivalent to of 41%–54% of excess body weight loss,[19] sleeve gastrectomy 20%–30%, with equivalent loss of 45%–64%,[19],[21] and RYGB approximately 35% with equivalent loss of 62%–75%, this loss being maintained at 10–14 years following surgery.[19],[20],[21],[22] RYGB, the more invasive procedure, is associated with greater long-term success but higher short-term morbidity in comparison with the less invasive ones, such as LAGB. In April 2013 various regulatory bodies including the American Association of Clinical Endocrinologists (AACE), The Obesity Society, and American Society for Metabolic and Bariatric surgery have recommended bariatric surgery for (1) All patients with a BMI ≥40 kg/m 2 without coexisting medical problems, and (2) patients with a BMI ≥35 kg/m 2 with presence of one or more obesity-related comorbidities, including type 2 diabetes, hypertension, hyperlipidemia, obstructive sleep apnea, hypoventilation syndrome, debilitating arthritis, severe urinary incontinence, venous stasis, fatty liver disease, gastroesophageal reflux disease (GERD), or with considerably impaired quality of life.[18]

The choice of procedure is dictated by the degree of obesity or BMI. LAGB is the procedure of choice in individuals with a BMI >30 kg/m 2, whereas RYGB in those with BMI >35 kg/m 2. Besides improving the quality of life, bariatric surgeries have also shown to improve the psychiatric dysfunction seen in obese patients when compared with only minor and sporadic improvement in medically treated patients.[25]


   Complications of Bariatric Surgery Top


Although significant improvement is seen with weight loss along with decrease in comorbid conditions, there is growing concern that bariatric surgery exerts negative effects on individuals' health. Due to the high volume of bariatric surgeries being performed routinely, safety prior to and after the surgery has become an issue of utmost priority. Many guidelines and criteria related to the accreditation of obesity management centers and careful monitoring of outcomes have thus been released.[18],[26],[27],[28] The US Bariatric Outcomes Longitudinal Database reported 1-year complication rates of 4.6%, 10.8%, 14.9%, and 25.7% respectively, following LAG placement, LSG, RYGB, and BPD.[27] In the long term, the contribution of nutritional factors is also of vital importance as growing evidence shows that all bariatric procedures are capable of producing significant nutritional and metabolic abnormalities.[28] Numerous factors are known to increase the risk of morbidity and mortality with different procedures in patients undergoing surgery. These factors include (1) older age, (2) male gender, (3) very high BMI, (4) presence of coexisting chronic diseases,[29],[30] (5) the qualification and experience of the surgeons, (6) qualification and experience of the center and facilities available therein,[31],[32] and (7) surgeries using the open approach instead of the laparoscopic one.[33]

Complications that may arise include the immediate intraoperative, late, and metabolic complications. We focus on the nonsurgical aspects of perioperative aspect of the bariatric surgery patient, with special emphasis on hormonal and metabolic problems and management.

Short-term complications

The overall 30-day mortality postoperatively is shown to be less than 1% in general; however, it may range between 0.3% and 8%.[34],[35],[36] Wound infection, bleeding, deep venous thrombosis, and pulmonary embolism are the early complications of the surgery,[32] whereas pulmonary embolism and surgical leak are the most common causes of death.[37],[38]

Late complications

Late complications related to the surgical procedure include stomal stenosis, marginal ulcers, cholelithiasis, internal and incisional hernias, short bowel syndrome, nutritional deficiencies, and dumping syndrome.[19],[21],[22],[24],[39]

Metabolic complications

Metabolic complications of bariatric surgeries include metabolic acidosis, and/or alkalosis, electrolyte abnormalities including low calcium, potassium, magnesium, sodium, and phosphorus that may cause arrhythmias and/or myopathies. Nutritional abnormalities in the form of fat-soluble vitamin deficiencies involving A, D, E, and K, iron and folic acid deficiency, negative calcium balance, and vitamin D deficiency causing secondary hyperparathyroidism, oxalosis, kidney stones, thiamine deficiency, vitamin B12 deficiency, increased bacterial overgrowth causing nocturnal diarrhea and abdominal distension, have been documented.[37],[40],[41],[42],[43],[44],[45] Periodic measurement of electrolytes, minerals, and vitamins, and replacing deficiencies if any will result in better management of metabolic complications.

In this article, we will review more specifically the hypoglycemia and osteoporosis after bariatric surgery in greater details, as these are the most severe and difficult to manage.

Hypoglycemia

Hypoglycemia is increasingly being recognized as a complication of gastric bypass surgeries. Relative risk of hypoglycemia increases sevenfold in the postgastric bypass population,[46] and the frequency of asymptomatic documented hypoglycemia after oral glucose tolerance test reached 30% among postgastric bypass patients.[47] A median time from surgery to development of symptoms was observed to be 2.7 years (few weeks after surgery to 5 years).[48] The pathophysiology of hypoglycemia remains controversial; dumping syndrome, an increase in beta cell mass, alteration of beta cell function, and other factors not related to beta cell were all suggested as possible mechanisms.[34],[47],[48],[49],[50],[51],[52] Decreased storage capacity of the stomach and the lack of rate-limiting step to food delivery, directly into the small intestine results in an exaggerated release of insulin, eventually leading to reactive hypoglycemia. Dumping syndrome can occur in up to 50% of patients after surgery [22] along with an increase in insulin and C-peptide levels after meals.[53],[54] Levels of other hormones and peptides, namely, glucagon-like peptides (GLP-1), glucose-dependent insulinotropic polypeptide (GIP), peptide YY (PYY), cholecystokinin (CCK), ghrelin, gastrin, somatostatin, pancreatic polypeptide (PP), amylin, and leptin were studied in relation to this. The studies found high concentrations of GLP-1 and PYY and a lower level of ghrelin, leptin, acylation-stimulating hormone, and visfatin.[54],[55] Amplification of GLP-1 levels were attributed to the anatomical alteration of the gastrointestinal tract, resulting in dysfunction as well as hypertrophy of the beta cells causing overstimulation and prolonged secretion of insulin and a decrease in glucagon release. This proposed mechanism is one of the more accepted theories for the development of hypoglycemia in these patients. In addition, increased weight loss following surgery along with an increase in insulin sensitivity may additionally contribute to development of hypoglycemia. Service et al. and Patti et al. described cases of noninsulinoma pancreatogenous hypoglycemia syndrome (NIPHS) that presented with symptoms of postprandial neuroglycopenia secondary to hyperinsulinemic hypoglycemia. In their series, the diagnosis of NIPHS was confirmed pathologically by the presence of diffused islet hypertrophy or nesidioblastosis in pancreas.[56],[57] Nevertheless, besides NIPHS other differential diagnosis of hypoglycemia, including insulinoma, factitious insulin or sulfonylurea administration, adrenal insufficiency, insulin autoimmune hypoglycemia, and tumor-producing insulin-like hormone or peptides must be considered.[58]

Clinical presentation varies from asymptomatic to mild neurogenic, to more severe neuroglycopenic symptoms. The neurogenic or adrenergic symptoms include tremor, tachycardia, diaphoresis, anxiety, and a sensation of hunger. The neuroglycopenic symptoms include weakness, tiredness, or dizziness, inappropriate behavior, difficulty with concentration, confusion, blurred vision, and in severe cases, it may lead to coma and death. Most of the patients tend to have mild adrenergic post-prandial symptoms, whereas a few may have severe and refractory symptoms that require pharmacological and/or surgical interventions.[59] The diagnosis is classically based on the presence of hypoglycemic symptoms that are ameliorated by taking glucose, and a laboratory-based documentation of low plasma glucose (<55 mg/dL) (Whipple's triad). Hypoglycemia associated with dumping syndrome presents soon after surgery with vasomotor symptoms followed by symptoms of hypoglycemia 2–3 h after the meal.[60] In contrast to dumping syndrome, patients with autonomous hyperinsulinemia, arising due to alterations in beta cell mass and/or function, present late, one year or more postsurgery, without the early vasomotor symptoms.[61]

Patients with mild adrenergic post-postprandial symptoms can be managed by dietary advises without any further workup.[59] AACE/TOS/ASMBS recommends that patients presenting with postprandial hypoglycemic symptoms severe or unresponsive to nutritional manipulation should undergo an evaluation to differentiate NIPHS from factitious or iatrogenic causes, dumping syndrome, and insulinoma. Cases of insulinoma have also been reported to occur postbariatric surgeries [62] with 10% of cases presenting with symptoms of postprandial hypoglycemia.[63] Supervised prolonged fasting (72 h fasting test) is usually indicated to rule out insulinoma. Additionally, the use of continuous glucose monitoring can also be employed to determine low interstitial fluid glucose at the time of symptoms, whereas provocative testing to induce hypoglycemia using oral glucose tolerance test (OGTT) and mixed-meal studies are less commonly used techniques. Further confirmatory tests using imaging studies such as triple-phase spiral computed tomography, magnetic resonance imaging, and transabdominal ultrasound of the pancreas, should also be undertaken. Additionally, selective arterial calcium-stimulation test is employed as the last step in the evaluation of these patients to localize the area of hypersecretion.[64]

The modality of treating hypoglycemia postbariatric surgery depends on the severity of the symptoms and the response of the patient to the initial dietary recommendations. Patients with early postoperative mild adrenergic post-postprandial symptoms can be managed initially with dietary advises including frequent, small meals and low-carbohydrate diet.[59] For resistant cases, or presenting later postoperative and those with severe hypoglycemia require further evaluation and therapy. In patients who do not respond well to the dietary modification pharmacological therapy can be initiated with acarbose, diazoxide, verapamil, and somatostatin.[65],[66],[67]

Acarbose, which is an α-glucosidase inhibitor (AGI), acts by reducing the glucose load in the jejunum thereby inhibiting the main stimulus for GLP-1 secretion. Studies in patients with dumping syndrome showed that acarbose produced a fivefold decrease in postprandial GLP-1 levels,[68] whereas in post-RYGBP patients an ingestion of acarbose 15 mins after a meal reduced serum insulin and GLP-1 levels and ameliorated symptoms of hypoglycemia.[69] The common side effects of this treatment include diarrhea, abdominal pain, and increased frequency and intensity of flatulence.

Diazoxide is the firstline drug for management of hyperinsulenimic hypoglycemia. It acts by opening the potassium ATP channels and preventing glucose-stimulated insulin secretion. Diazoxide responsiveness is determined by (1) appropriate fasting tolerance for age; (2) feed volume and frequency normal for age; and (3) normal blood sugar levels at the end of the fast. Patients can have hypotension, anxiety, dizziness, headache, insomnia, anorexia, and diarrhea as side effects of this medication.[66]

Verapamil is a calcium channel blocker that acts by inhibiting calcium ion from entering pancreatic cells and therefore inhibits insulin secretion. Common side effects include headache, gastrointestinal disturbance, peripheral edema, and hypotension.[66]

Octreotide, a somatostatin analog, is the other drug that can be used for the treatment of hypoglycemia. Besides its inhibiting action on growth hormone (GH), glucagon and insulin it also inhibits release of several gastrointestinal hormones, including serotonin, gastrin, vasoactive intestinal peptide, secretin, motilin, and pancreatic polypeptide. The criteria for responsiveness to octreotide are similar to those for diazoxide, and its common side effects include sinus bradycardia, fatigue, headache, abdominal pain, nausea, diarrhea, and cholelithiasis.[70]

In cases where medical treatment fails, surgical intervention is advocated through reversal of the bariatric procedure, employing postoperative feeding to the bypassed proximal gut by gastrostomy tube followed by partial pancreatic resection in refractory cases.[71]

Metabolic bone disease

Another complication of increasing concern arising as a consequence of bariatric surgery is metabolic bone disease that leads up to osteoporosis and osteoporotic fracture. Overweight and obesity have been considered in the past to exert a protective effect on the bones due to the loading effect. Both conditions in fact are associated with increased incidence of vitamin D (60%–86%) and calcium deficiencies with elevated parathyroid hormone (PTH) levels placing them at risk of low bone mass and metabolic bone disease, including osteoporosis.[72] In their study of 279 morbid obese Carli et al. found that 60% of cases were deficient in vitamin D and 48% had secondary hyperparathyroidism.[73] Increased weight due to mechanical loading effect, negatively affects the skeleton by accelerating bone loss, thereby increasing bone fragility.[74] The pathophysiology of bone disease in the obese patients is multifactorial ranging from inadequate nutrition due to chronic dieting practices, lack of physical activity, and increased sequestration of vitamin D within the adipocytes. Bone metabolism depends normally on an adequate dietary intake of calcium and phosphorus regulated by parathyroid hormone, vitamin D, and FGF23. It is also affected by a complex network of local neuronal and hormonal factors, including gastrointestinal hormones whose role has been proposed based on evidence that bone resorption dramatically falls after a meal.

The impact of major weight loss on bone metabolism after bariatric surgery was until recently considered to be the sole result of a combination of mechanical and nutritional effects. The notion changed with recent insights, which showed an intricate and complex interplay between the signaling factors of gut, bone, and fat tissue. This interplay forms the basis of convergence of bone and energy metabolism utilizing a third neurohormonal mechanism regulating bone turnover through adipokines; leptin and adiponectin, gonadal steroids,[75] and gut-derived hormones; serotonin, ghrelin, PYY, GIP, and GLP-1, GLP-2.[76] GIP's receptor, glucose-dependent insulinotropic polypeptide receptor (GIPR), is expressed in bone tissue and its deficiency in animals reportedly led to increased bone resorption with a pronounced reduction in the degree of mineralization of bone matrix.[77]

Alterations of the adipokines and incretins after bariatric surgery has significant negative effect on bone metabolism and health [78] and further compounds the already existing metabolic bone disease in obese individuals. The degree of bone loss or disease varies with the type of surgery undertaken. Surgeries employing malabsorptive techniques such as RYGB, bypass the primary absorption sites for vitamins and minerals, that is, the duodenum and proximal jejunum resulting in deficiencies of key osteogenic factors such as calcium that is actively absorbed from the proximal foregut, and vitamin D that requires bile acids and pancreatic secretions for optimal absorption. Restrictive techniques, such as sleeve gastrectomy, on the other hand reduce the total amount of gastric acid required for lowering the pH for optimal absorption of other essential vitamins and minerals. RYGB and biliopancreatic diversion can thus cause malabsorption of calcium (25%–50%) and vitamin D (>50%) and other nutrients—protein, folate, iron, magnesium, thiamine, B12, and vitamin A—that are essential for bone health. In turn, the intensity or degree of these micronutrient deficiencies varies depending on the length of intestine bypassed. Numerous reported cases clearly show the risk of metabolic bone disease occurring from as early as 8 weeks until 32 years after bariatric surgery.[79] The percentage of bone lost also correlates strongly with how fast the weight is lost. A recent study found that losing 0.7 kg/week was more detrimental to bone than a slower loss of 0.3 kg/week due to the activation of the calcium–PTH axis.[80] After bariatric surgery, many patients rapidly lose 50–100 kg of their weight; this weight loss combined with severely restricted oral intake of all the nutrients that includes proteins, calcium, and vitamins predisposes them to furthering the development of metabolic bone disease.[81]

Alterations in the levels of the adipokines also affect the outcomes of the surgical procedures. After RYGP, adiponectin levels were shown to increase while leptin levels decreased in proportion to loss of total body fat;[82] and GIP levels, fasting and postprandial, were found to be reduced only in diabetic patients. The levels of incretins, total GLP-1 and PYY, increased after RYGB, BPD,[83] LAG,[84] and LSG [85] as early as 1–6 weeks postsurgery and remained elevated for at least 1 year,[86],[87] whereas the pancreatic polypeptide response decreased. Nannipieri et al. found that at 1-year, levels of PYY were increased, and pancreatic, amylin, ghrelin, and GLP-1 were reduced in RYGB and LSG except for PP and amylin, which were increased and unchanged in LSG group.[88] Ghrelin levels were shown to decrease at 1 and 12 months after RYGB surgery with subsequent improvements after 12 months postsurgery correlating strongly with weight loss and increased insulin sensitivity.[89] The effect of surgery on ghrelin levels remains uncertain, although few studies have reported postoperative decreases in its levels in RYGB and gastric sleeve.[90] In addition to gut hormones, locally synthesized hormones such as the estrogens, known to impact bone health were also altered post operatively. As weight decreases and adipose stores are depleted, the levels of estrogen decrease in both men and women resulting in decreased impact of estrogen on bone. Estrogen may also affect bone metabolism by direct effects on vitamin D and calcium metabolism.[91]

Von Mach et al. in their study reported a significant decrease in the bone mineral content of patients undergoing RYGB accompanied by significant increases in levels of markers of bone turnover, namely, urinary deoxypyridinoline and in serum osteocalcin 24 months after RYGB, suggesting both, increased bone resorption and a parallel decreased bone formation.[92]

The investigations generally should include serum and urine calcium, 25-hydroxyvitamin D, alkaline phosphatase, and serum intact PTH levels. An increase in serum intact PTH level is indicative of negative calcium balance or a vitamin D deficiency (or both), whereas elevations of bone-specific alkaline phosphatase level, which is indicative of increased osteoblastic activity and bone formation, are often the initial abnormalities. Complications may be seen as early as 8 weeks after bariatric surgery in the form of secondary hyperparathyroidism and osteomalacia.[93],[94] Meticulous preoperative screening, judicious use of vitamin and mineral supplements, addressing modifiable risk factors, and monitoring the absorption of key nutrients postoperatively are essential in preventing metabolic bone disease in bariatric surgery patients. The American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic and Bariatric Surgery AACE/TOS/ASMBS guidelines [95] recommends performing certain laboratory tests every three months in the first year after surgery, and every 3–12 months thereafter, depending on symptoms [Table 1].
Table 1: Association of Clinical Endocrinologists, the Obesity Society, and American Society for Metabolic and Bariatric Surgery (AACE/TOS/ASMBS) recommendations of periodic laboratory tests postbariatric surgery

Click here to view


Dual-energy X-ray absorptiometry (DXA) is accepted as a marker of bone strength, fracture risk, and an important tool that can be used to assess the bone mineral density of individuals and to identify the presence of osteoporosis. DXA of the hip and spine is a common modality used to diagnose osteoporosis in men over age 50 years and postmenopausal women, whereas in younger patients the levels serve as baseline measurement for future comparison. DXA assessment should be carried out in both men and women prior to and after bariatric surgery. The markers of bone resorption also showed significant elevations in osteocalcin and bone alkaline phosphatase levels.[96] One year following the RYGB, bone mass density declined at femoral neck by 9.2%–10.9%, at total hip by 8%–10%, and in lumbar spine by 3.6%–7.4%.[92] Exclusively, restrictive procedures such as gastric banding formerly considered not to impact bone health and metabolism are now known to place patients at risk for metabolic bone disease due to the inadequate intake of calcium and vitamin D in the immediate postoperative period. Pugnale et al. found that 48% of patients had more than 3% statistically significant bone mineral reduction 12 months after undergoing gastric banding.[97] Seventy percent of patients undergoing malabsorptive procedure also developed osteomalacia, with elevations in markers of bone resorption as early as 8 weeks after bariatric surgery.[94]

Nakamuro et al. in their cohort with a majority of middle-aged morbidly obese (BMI was 49 ± 8 kg/m 2) female participants followed up for a median of 7.7 years, documented a 2.3-fold increase in the relative risk for any fracture at the common osteoporotic sites (hip, spine, wrist, and humerus). Incidences of fractures were seen early after surgery till as late as 5 years.[96]

Postoperatively, many bariatric patients require chewable or liquid supplements to facilitate adequate absorption. The AACE-recommended treatment guidelines for these patients include postsurgery replacement of calcium and vitamin D [Table 2].
Table 2: American Association of Clinical Endocrinologists recommendation for replacement of calcium and vitamin D postbariatric surgery

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In patients who require pharmacological therapy for osteoporosis, treatment can be initiated, if the vitamin D and calcium levels are normal or after therapeutic correction of insufficiency, with the use of bisphosphonates. In cases where therapy is indicated, intravenously administered bisphosphonates should be used, as there are concerns about inadequate oral absorption and potential anastomotic ulceration with orally administered bisphosphonates.[98]


   Conclusion Top


Bariatric surgery is the most effective therapeutic option for obese patients; however, it carries substantial risks including procedure-related complications, malabsorption, and hormonal disturbance. Preoperative assessment and then regular follow up postoperatively by an endocrinologist or obesity-specialized internist is crucial. In addition, patients must be aware of the multiple risks and the need for regular assessment and follow up by specialized physicians. Dietary instructions and vitamins and mineral supplements must be initiated early on to prevent major consequences.

 
   References Top

1.
Obesity and Overweight. The World Health Organization. Available at: http://www.who.int/mediacentre/factsheets/fs311/en/. [Last updated 2015 Jan].  Back to cited text no. 1
    
2.
Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA 2006;295:1549-55.  Back to cited text no. 2
    
3.
Al-Nozha MM, Al-Mazrou YY, Al-Maatouq MA, Arafah MR, Khalil MZ, Khan NB, et al. Obesity in Saudi Arabia. Saudi Med J 2005;26:824-9.  Back to cited text no. 3
    
4.
Obesity: Preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 2000;894:i-xii, 1-253.  Back to cited text no. 4
    
5.
Willett WC, Dietz WH, Colditz GA. Guidelines for healthy weight. N Engl J Med 1999;341:427-34.  Back to cited text no. 5
    
6.
Field AE, Coakley EH, Must A, Spadano JL, Laird N, Dietz WH, et al. Impact of overweight on the risk of developing common chronic diseases during a 10-year period. Arch Intern Med 2001;161:1581-6.  Back to cited text no. 6
    
7.
Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: A systematic review and meta-analysis of prospective observational studies. Lancet 2008;371:569-78.  Back to cited text no. 7
    
8.
Romero-Corral A, Montori VM, Somers VK, Korinek J, Thomas RJ, Allison TG, et al. Association of bodyweight with total mortality and with cardiovascular events in coronary artery disease: A systematic review of cohort studies. Lancet 2006;368:666-78.  Back to cited text no. 8
    
9.
Whitlock G, Lewington S, Sherliker P, Clarke R, Emberson J, Halsey J, et al.; Prospective Studies Collaboration. Body-mass index and cause-specific mortality in 900 000 adults: Collaborative analyses of 57 prospective studies. Lancet 2009;373:1083-96.  Back to cited text no. 9
    
10.
Fontaine KR, Redden DT, Wang C, Westfall AO, Allison DB. Years of life lost due to obesity. JAMA 2003;289:187-93.  Back to cited text no. 10
    
11.
Brolin RE. Update: NIH consensus conference. Gastrointestinal surgery for severe obesity. Nutrition 1996;12:403-4.  Back to cited text no. 11
    
12.
Gloy VL, Briel M, Bhatt DL, Kashyap SR, Schauer PR, Mingrone G, et al. Bariatric surgery versus non-surgical treatment for obesity: A systematic review and meta-analysis of randomised controlled trials. BMJ 2013;347:f5934.  Back to cited text no. 12
    
13.
Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, et al. Weight and type 2 diabetes after bariatric surgery: Systematic review and meta-analysis. Am J Med 2009;122:248-56.e5.  Back to cited text no. 13
    
14.
Christou NV, Sampalis JS, Liberman M, Look D, Auger S, McLean AP, et al. Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients. Ann Surg 2004;240:416-24.  Back to cited text no. 14
    
15.
Sjöström L, Narbro K, Sjöström CD, Karason K, Larsson B, Wedel H, et al.; Swedish Obese Subjects Study. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 2007;357:741-52.  Back to cited text no. 15
    
16.
Adams TD, Gress RE, Smith SC, Halverson RC, Simper SC, Rosamond WD, et al. Long-term mortality after gastric bypass surgery. N Engl J Med 2007;357:753-61.  Back to cited text no. 16
    
17.
Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM, et al.; American Association of Clinical Endocrinologists; Obesity Society; American Society for Metabolic and Bariatric Surgery. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient—2013 update: Cosponsored by American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic and Bariatric Surgery. Obesity (Silver Spring) 2013;21(Suppl 1):S1-27.  Back to cited text no. 17
    
18.
Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM, et al.; American Association of Clinical Endocrinologists; Obesity Society; American Society for Metabolic and Bariatric Surgery. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient--2013 update: Cosponsored by American Association of Clinical Endocrinologists, the Obesity Society, and American Society for Metabolic and Bariatric Surgery. Endocr Pract 2013;19:337-72.  Back to cited text no. 18
    
19.
Nasr SH, D'Agati VD, Said SM, Stokes MB, Largoza MV, Radhakrishnan J, et al. Oxalate nephropathy complicating Roux-en-Y Gastric Bypass: An underrecognized cause of irreversible renal failure. Clin J Am Soc Nephrol 2008;3:1676-83.  Back to cited text no. 19
    
20.
Lockhart ME, Tessler FN, Canon CL, Smith JK, Larrison MC, Fineberg NS, et al. Internal hernia after gastric bypass: Sensitivity and specificity of seven CT signs with surgical correlation and controls. AJR Am J Roentgenol 2007;188:745-50.  Back to cited text no. 20
    
21.
Skroubis G, Anesidis S, Kehagias I, Mead N, Vagenas K, Kalfarentzos F. Roux-en-Y gastric bypass versus a variant of biliopancreatic diversion in a non-superobese population: Prospective comparison of the efficacy and the incidence of metabolic deficiencies. Obes Surg 2006;16:488-95.  Back to cited text no. 21
    
22.
McBride CL, Petersen A, Sudan D, Thompson J. Short bowel syndrome following bariatric surgical procedures. Am J Surg 2006;192:828-32.  Back to cited text no. 22
    
23.
Ukleja A. Dumping syndrome: Pathophysiology and treatment. Nutr Clin Pract 2005;20:517-25.  Back to cited text no. 23
    
24.
Angrisani L, Lorenzo M, Borrelli V. Laparoscopic adjustable gastric banding versus Roux-en-Y gastric bypass: 5-year results of a prospective randomized trial. Surg Obes Relat Dis 2007;3:127-33.  Back to cited text no. 24
    
25.
Sjöström L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, et al.; Swedish Obese Subjects Study Scientific Group. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 2004;351:2683-93.  Back to cited text no. 25
    
26.
Schirmer B, Jones DB. The American College of Surgeons Bariatric Surgery Center Network: Establishing standards. Bull Am Coll Surg 2007;92:21-7.  Back to cited text no. 26
    
27.
Demaria EJ, Winegar DA, Pate VW, Hutcher NE, Ponce J, Pories WJ. Early postoperative outcomes of metabolic surgery to treat diabetes from sites participating in the ASMBS bariatric surgery center of excellence program as reported in the Bariatric Outcomes Longitudinal Database. Anna Surg 2010;252:559-67.  Back to cited text no. 27
    
28.
Welbourn R, Pournaras D. Bariatric surgery: A cost-effective intervention for morbid obesity; functional and nutritional outcomes. Proc Nutr Soc 2010;69:528-35.  Back to cited text no. 28
    
29.
Livingston EH, Langert J. The impact of age and Medicare status on bariatric surgical outcomes. Arch Surg 2006;141:1115-21.  Back to cited text no. 29
    
30.
Arterburn D, Livingston EH, Schifftner T, Kahwati LC, Henderson WG, Maciejewski ML. Predictors of long-term mortality after bariatric surgery performed in Veterans Affairs medical centers. Arch Surg 2009;144:914-20.  Back to cited text no. 30
    
31.
Hollenbeak CS, Rogers AM, Barrus B, Wadiwala I, Cooney RN. Surgical volume impacts bariatric surgery mortality: A case for centers of excellence. Surgery 2008;144:736-43.  Back to cited text no. 31
    
32.
Schauer P, Ikramuddin S, Hamad G, Gourash W. The learning curve for laparoscopic Roux-en-Y gastric bypass is 100 cases. Surg Endosc 2003;17:212-5.  Back to cited text no. 32
    
33.
Nguyen NT, Goldman C, Rosenquist CJ, Arango A, Cole CJ, Lee SJ, et al. Laparoscopic versus open gastric bypass: A randomized study of outcomes, quality of life, and costs. Ann Surg 2001;234:279-91.  Back to cited text no. 33
    
34.
Flum DR, Belle SH, King WC, Wahed AS, Berk P, Chapman W, et al.; Longitudinal Assessment of Bariatric Surgery (LABS) Consortium. Perioperative safety in the longitudinal assessment of bariatric surgery. N Engl J Med 2009;361:445-54.  Back to cited text no. 34
    
35.
DeMaria EJ, Portenier D, Wolfe L. Obesity surgery mortality risk score: Proposal for a clinically useful score to predict mortality risk in patients undergoing gastric bypass. Surg Obes Relat Dis 2007;3:134-40.  Back to cited text no. 35
    
36.
DeMaria EJ, Murr M, Byrne TK, Blackstone R, Grant JP, Budak A, et al. Validation of the obesity surgery mortality risk score in a multicenter study proves it stratifies mortality risk in patients undergoing gastric bypass for morbid obesity. Ann Surg 2007;246:578-84.  Back to cited text no. 36
    
37.
Lancaster RT, Hutter MM. Bands and bypasses: 30-day morbidity and mortality of bariatric surgical procedures as assessed by prospective, multi-center, risk-adjusted ACS-NSQIP data. Surg Endosc 2008;22:2554-63.  Back to cited text no. 37
    
38.
Melinek J, Livingston E, Cortina G, Fishbein MC. Autopsy findings following gastric bypass surgery for morbid obesity. Arch Pathol Lab Med 2002;126:1091-5.  Back to cited text no. 38
    
39.
Fishbein TM. Intestinal transplantation. N Engl J Med 2009;361:998-1008.  Back to cited text no. 39
    
40.
Dolan K, Hatzifotis M, Newbury L, Lowe N, Fielding G. A clinical and nutritional comparison of biliopancreatic diversion with and without duodenal switch. Ann Surg 2004;240:51-6.  Back to cited text no. 40
    
41.
Mechanick JI, Bergman DA, Braithwaite SS, Palumbo PJ; American Association of Clinical Endocrinologists Ad Hoc Task Force for Standardized Production of Clinical Practice Guidelines. American Association of Clinical Endocrinologists protocol for standardized production of clinical practice guidelines. Endocr Pract 2004;10:353-61.  Back to cited text no. 41
    
42.
Bloomberg RD, Fleishman A, Nalle JE, Herron DM, Kini S. Nutritional deficiencies following bariatric surgery: What have we learned? Obes Surg 2005;15:145-54.  Back to cited text no. 42
    
43.
Fujioka K. Follow-up of nutritional and metabolic problems after bariatric surgery. Diabetes Care 2005;28:481-4.  Back to cited text no. 43
    
44.
Mason ME, Jalagani H, Vinik AI. Metabolic complications of bariatric surgery: Diagnosis and management issues. Gastroenterol Clin North Am 2005;34:25-33.  Back to cited text no. 44
    
45.
Alvarez-Leite JI. Nutrient deficiencies secondary to bariatric surgery. Curr Opin Clin Nutr Metab Care 2004;7:569-75.  Back to cited text no. 45
    
46.
Gonzalez-Campoy JM, St Jeor ST, Castorino K, Ebrahim A, Hurley D, Jovanovic L, et al.; American Association of Clinical Endocrinologists; AmericanCollege of Endocrinology and the Obesity Society. Clinical practice guidelines for healthy eating for the prevention and treatment of metabolic and endocrine diseases in adults: Cosponsored by the American Association of Clinical Endocrinologists/the American College of Endocrinology and the Obesity Society. Endocr Pract 2013;19(Suppl 3):1-82.  Back to cited text no. 46
    
47.
Kim SH, Liu TC, Abbasi F, Lamendola C, Morton JM, Reaven GM, et al. Plasma glucose and insulin regulation is abnormal following gastric bypass surgery with or without neuroglycopenia. Obes Surg 2009;19:1550-6.  Back to cited text no. 47
    
48.
Marsk R, Jonas E, Rasmussen F, Näslund E. Nationwide cohort study of post-gastric bypass hypoglycaemia including 5,040 patients undergoing surgery for obesity in 1986-2006 in Sweden. Diabetologia 2010;53:2307-11.  Back to cited text no. 48
    
49.
Vella A, Service FJ. Incretin hypersecretion in post-gastric bypass hypoglycemia—Primary problem or red herring? J Clin Endocrinol Metab 2007;92:4563-5.  Back to cited text no. 49
    
50.
Patti ME, Goldfine AB. Hypoglycaemia following gastric bypass surgery—Diabetes remission in the extreme? Diabetologia 2010;53:2276-9.  Back to cited text no. 50
    
51.
Scavini M, Pontiroli AE, Folli F. Asymptomatic hyperinsulinemic hypoglycemia after gastric banding. N Engl J Med 2005;353:2822-3.  Back to cited text no. 51
    
52.
Holst JJ. Glucagonlike peptide 1: A newly discovered gastrointestinal hormone. Gastroenterology 1994;107:1848-55.  Back to cited text no. 52
    
53.
Deitel M. The change in the dumping syndrome concept. Obes Surg 2008;18:1622-4.  Back to cited text no. 53
    
54.
Cui Y, Elahi D, Andersen DK. Advances in the etiology and management of hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass. J Gastrointest Surg 2011;15:1879-88.  Back to cited text no. 54
    
55.
Jacobsen SH, Olesen SC, Dirksen C, Jorgensen NB, Bojsen-Møller KN, Kielgast U, et al. Changes in gastrointestinal hormone responses, insulin sensitivity, and beta-cell function within 2 weeks after gastric bypass in non-diabetic subjects. Obes Surg 2012;22:1084-96.  Back to cited text no. 55
    
56.
Service GJ, Thompson GB, Service FJ, Andrews JC, Collazo-Clavell ML, Lloyd RV. Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery. N Engl J Med 2005;353:249-54.  Back to cited text no. 56
    
57.
Meier JJ, Nauck MA, Butler PC. Comment to: Patti ME, McMahon G, Mun EC, et al. (2005) Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: Evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia 48:2236-40. Diabetologia 2006;49:607-10.  Back to cited text no. 57
    
58.
Zagury L, Moreira RO, Guedes EP, Coutinho WF, Appolinario JC. Insulinoma misdiagnosed as dumping syndrome after bariatric surgery. Obes Surg 2004;14:120-3.  Back to cited text no. 58
    
59.
Cryer PE, Axelrod L, Grossman AB, Heller SR, Montori VM, Seaquist ER, et al. Evaluation and management of adult hypoglycemic disorders: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 2009;94:709-28.  Back to cited text no. 59
    
60.
Foster-Schubert KE. Hypoglycemia complicating bariatric surgery: Incidence and mechanisms. Curr Opin Endocrinol Diabetes Obes 2011;18:129-33.  Back to cited text no. 60
    
61.
Bantle JP, Ikramuddin S, Kellogg TA, Buchwald H. Hyperinsulinemic hypoglycemia developing late after gastric bypass. Obes Surg 2007;17:592-4.  Back to cited text no. 61
    
62.
Abellán P, Cámara R, Merino-Torres JF, Pérez-Lazaro A, del Olmo MI, Ponce JL, et al. Severe hypoglycemia after gastric bypass surgery for morbid obesity. Diabetes Res Clin Pract 2008;79:e7-9.  Back to cited text no. 62
    
63.
Placzkowski KA, Vella A, Thompson GB, Grant CS, Reading CC, Charboneau JW, et al. Secular trends in the presentation and management of functioning insulinoma at the Mayo Clinic, 1987-2007. J Clin Endocrinol Metab 2009;94:1069-73.  Back to cited text no. 63
    
64.
Singh E, Vella A. Hypoglycemia after gastric bypass surgery. Diabetes Spectr 2012;25:217-21.  Back to cited text no. 64
    
65.
Kellogg TA, Bantle JP, Leslie DB, Redmond JB, Slusarek B, Swan T, et al. Postgastric bypass hyperinsulinemic hypoglycemia syndrome: Characterization and response to a modified diet. Surg Obes Relat Dis 2008;4:492-9.  Back to cited text no. 65
    
66.
Moreira RO, Moreira RB, Machado NA, Gonçalves TB, Coutinho WF. Post-prandial hypoglycemia after bariatric surgery: Pharmacological treatment with verapamil and acarbose. Obes Surg 2008;18:1618-21.  Back to cited text no. 66
    
67.
Spanakis E, Gragnoli C. Successful medical management of status post-Roux-en-Y-gastric-bypass hyperinsulinemic hypoglycemia. Obes Surg 2009;19:1333-4.  Back to cited text no. 67
    
68.
Imhof A, Schneemann M, Schaffner A, Brändle M. Reactive hypoglycaemia due to late dumping syndrome: Successful treatment with acarbose. Swiss Med Wkly 2001;131:81-3.  Back to cited text no. 68
    
69.
Valderas JP, Ahuad J, Rubio L, Escalona M, Pollak F, Maiz A. Acarbose improves hypoglycaemia following gastric bypass surgery without increasing glucagon-like peptide 1 levels. Obes Surg 2012;22:582-6.  Back to cited text no. 69
    
70.
Mohamed Z, Arya VB, Hussain K. Hyperinsulinaemic hypoglycaemia: Genetic mechanisms, diagnosis and management. J Clin Res Pediatr Endocrinol 2012;4:169-81.  Back to cited text no. 70
    
71.
Cui Y, Elahi D, Andersen DK. Advances in the etiology and management of hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass. J Gastrointest Surg 2011;15:1879-88.  Back to cited text no. 71
    
72.
Hsu YH, Venners SA, Terwedow HA, Feng Y, Niu T, Li Z, et al. Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 2006;83:146-54.  Back to cited text no. 72
    
73.
Carlin AM, Rao DS, Meslemani AM, Genaw JA, Parikh NJ, Levy S, et al. Prevalence of vitamin D depletion among morbidly obese patients seeking gastric bypass surgery. Surg Obes Relat Dis 2006;2:98-104.  Back to cited text no. 73
    
74.
Goldner WS, O'Dorisio TM, Dillon JS, Mason EE. Severe metabolic bone disease as a long-term complication of obesity surgery. Obes Surg 2002;12:685-92.  Back to cited text no. 74
    
75.
Hammoud A, Gibson M, Hunt SC, Adams TD, Carrell DT, Kolotkin RL, et al. Effect of Roux-en-Y gastric bypass surgery on the sex steroids and quality of life in obese men. J Clin Endocrinol Metab 2009;94:1329-32.  Back to cited text no. 75
    
76.
Hage MP, El-Hajj Fuleihan G. Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporos Int 2014;25:423-39.  Back to cited text no. 76
    
77.
Mieczkowska A, Irwin N, Flatt PR, Chappard D, Mabilleau G. Glucose-dependent insulinotropic polypeptide (GIP) receptor deletion leads to reduced bone strength and quality. Bone 2013;56:337-42.  Back to cited text no. 77
    
78.
Folli F, Sabowitz BN, Schwesinger W, Fanti P, Guardado-Mendoza R, Muscogiuri G. Bariatric surgery and bone disease: From clinical perspective to molecular insights. Int J Obes (Lond) 2012;36:1373-9.  Back to cited text no. 78
    
79.
Riedt CS, Brolin RE, Sherrell RM, Field MP, Shapses SA. True fractional calcium absorption is decreased after Roux-en-Y gastric bypass surgery. Obesity (Silver Spring) 2006;14:1940-8.  Back to cited text no. 79
    
80.
Cifuentes M, Riedt CS, Brolin RE, Field MP, Sherrell RM, Shapses SA. Weight loss and calcium intake influence calcium absorption in overweight postmenopausal women. Am J Clin Nutr 2004;80:123-30.  Back to cited text no. 80
    
81.
Haria DM, Sibonga JD, Taylor HC. Hypocalcemia, hypovitaminosis d osteopathy, osteopenia, and secondary hyperparathyroidism 32 years after jejunoileal bypass. Endocr Pract 2005;11:335-40.  Back to cited text no. 81
    
82.
Garcia de la Torre N, Rubio MA, Bordiú E, Cabrerizo L, Aparicio E, Hernández C, et al. Effects of weight loss after bariatric surgery for morbid obesity on vascular endothelial growth factor-A, adipocytokines, and insulin. J Clin Endocrinol Metab 2008;93:4276-81.  Back to cited text no. 82
    
83.
Garcia-Fuentes E, Garrido-Sanchez L, Garcia-Almeida JM, Garcia-Arnes J, Gallego-Perales JL, Rivas-Marin J, et al. Different effect of laparoscopic Roux-en-Y gastric bypass and open biliopancreatic diversion of Scopinaro on serum PYY and ghrelin levels. Obes Surg 2008;18:1424-9.  Back to cited text no. 83
    
84.
Reinehr T, Roth CL, Schernthaner GH, Kopp HP, Kriwanek S, Schernthaner G. Peptide YY and glucagon-like peptide-1 in morbidly obese patients before and after surgically induced weight loss. Obes Surg 2007;17:1571-7.  Back to cited text no. 84
    
85.
Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK. Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy: A prospective, double blind study. Ann Surg 2008;247:401-7.  Back to cited text no. 85
    
86.
Papamargaritis D, le Roux CW, Sioka E, Koukoulis G, Tzovaras G, Zacharoulis D. Changes in gut hormone profile and glucose homeostasis after laparoscopic sleeve gastrectomy. Surg Obes Relat Dis 2013;9:192-201.  Back to cited text no. 86
    
87.
Steinert RE, Peterli R, Keller S, Meyer-Gerspach AC, Drewe J, Peters T, et al. Bile acids and gut peptide secretion after bariatric surgery: A 1-year prospective randomized pilot trial. Obesity (Silver Spring) 2013;21:E660-8.  Back to cited text no. 87
    
88.
Nannipieri M, Baldi S, Mari A, Colligiani D, Guarino D, Camastra S, et al. Roux-en-Y gastric bypass and sleeve gastrectomy: Mechanisms of diabetes remission and role of gut hormones. J Clin Endocrinol Metab 2013;98:4391-9.  Back to cited text no. 88
    
89.
Samat A, Malin SK, Huang H, Schauer PR, Kirwan JP, Kashyap SR. Ghrelin suppression is associated with weight loss and insulin action following gastric bypass surgery at 12 months in obese adults with type 2 diabetes. Diabetes Obes Metab 2013;15:963-6.  Back to cited text no. 89
    
90.
Tymitz K, Engel A, McDonough S, Hendy MP, Kerlakian G. Changes in ghrelin levels following bariatric surgery: Review of the literature. Obes Surg 2011;21:125-30.  Back to cited text no. 90
    
91.
Gallagher JC, Riggs BL, DeLuca HF. Effect of estrogen on calcium absorption and serum vitamin D metabolites in postmenopausal osteoporosis. J Clin Endocrinol Metab 1980;51:1359-64.  Back to cited text no. 91
    
92.
von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U. Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism 2004;53:918-21.  Back to cited text no. 92
    
93.
De Prisco C, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci 2005;329:57-61.  Back to cited text no. 93
    
94.
Collazo-Clavell ML, Jimenez A, Hodgson SF, Sarr MG. Osteomalacia after Roux-en-Y gastric bypass. Endocr Pract 2004;10:195-8.  Back to cited text no. 94
    
95.
Mechanick JI, Kushner RF, Sugerman HJ, Gonzalez-Campoy JM, Collazo-Clavell ML, Spitz AF, et al.;American Association of Clinical Endocrinologists; Obesity Society; American Society for Metabolic and Bariatric Surgery. American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic and Bariatric Surgery medical guidelines for clinical practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Obesity (Silver Spring) 2009;17(Suppl 1):S1-70, v.  Back to cited text no. 95
    
96.
Obinwanne KM, Riess KP, Kallies KJ, Mathiason MA, Manske BR, Kothari SN. Effects of laparoscopic Roux-en-Y gastric bypass on bone mineral density and markers of bone turnover. Surg Obes Relat Dis 2014;10:1056-62.  Back to cited text no. 96
    
97.
Pugnale N, Giusti V, Suter M, Zysset E, Héraïef E, Gaillard RC, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes Relat Metab Disord 2003;27:110-6.  Back to cited text no. 97
    
98.
Nakamura KM, Haglind EG, Clowes JA, Achenbach SJ, Atkinson EJ, Melton LJ 3rd, et al. Fracture risk following bariatric surgery: A population-based study. Osteoporos Int 2014;25:151-8.  Back to cited text no. 98
    

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DOI: 10.4103/1319-3767.164183

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