Metabolic bone changes after bariatric surgery: 2020 update, American Society for Metabolic and Bariatric Surgery Clinical Issues Committee position statement

Abstract

The following position statement is issued by the American Society for Metabolic and Bariatric Surgery (ASMBS) for the purpose of enhancing quality of care in metabolic and bariatric surgery. The ASMBS published the first position statement addressing metabolic bone changes after bariatric surgery in 2015 [[1]Kim J. Brethauer S. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee, position statement. Metabolic bone changes after bariatric surgery.Surg Obes Relat Dis. 2015; 11: 406-411Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar]. In this updated statement, interval suggestions for management are presented, which are derived from available knowledge, peer-reviewed scientific literature, and expert opinion regarding monitoring and treatment of metabolic bone changes after metabolic and bariatric surgery procedures. The statement will continue to be revised in the future should additional evidence become available. Obesity rates in adults have continued to increase over the last decade. According to the Centers for Disease Control and Prevention, the disease of obesity affects 39.8% of US adults, or about 93.3 million Americans [[2]Hales C.M. Carroll M.D. Fryar C.D. Ogden C.L. Prevalence of obesity among adults and youth: United States, 2015-2016. NCHS data brief, no 288. National Center for Health Statistics, Hyattsville, MD2017Google Scholar]. The ASMBS estimates that more than 24 million Americans have severe obesity. Metabolic and bariatric surgery remains the most effective and durable treatment for severe obesity and obesity-related co-morbidities. Despite the large-scale and far-ranging health benefits of these procedures, there are anatomic and metabolic consequences that necessitate adherence to life-long micronutrient supplementation and monitoring, as well as potential unintended adverse effects, including those on bone health. Metabolic and bariatric surgery is associated with bone metabolism disorders, acceleration of bone remodeling, bone turnover, and bone loss, with decreased bone mineral density (BMD) [[1]Kim J. Brethauer S. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee, position statement. Metabolic bone changes after bariatric surgery.Surg Obes Relat Dis. 2015; 11: 406-411Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar]. The intent of this updated statement is to review the current evidence regarding bone loss after bariatric surgery and to provide interval recommendations. It is understood that any protective benefits of obesity against osteoporosis secondary to increased BMD (attributed to increases in mechanical loading, larger bone size, and increased aromatization of androgens from adipose tissue and adipokines [[3]Gómez J.M. Vilarrasa N. Masdevall C. et al.Regulation of bone mineral density in morbidly obese women: a cross-sectional study in two cohorts before and after bypass surgery.Obes Surg. 2009; 19: 345-350Crossref PubMed Scopus (34) Google Scholar,[4]Gómez-Ambrosi J. Rodríguez A. Catalán V. Frühbeck G. The bone-adipose axis in obesity and weight loss.Obes Surg. 2008; 18: 1134-1143Crossref PubMed Scopus (120) Google Scholar]) may be limited by the prevalence of high levels of preexisting vitamin D deficiencies—namely, 25-hydroxyvitamin D (25-OHD) and elevated parathyroid hormone (PTH) levels—with additional variations based on race, sex, and age [[5]Grethen E. McClintock R. Gupta C.E. et al.Vitamin D and hyperparathyroidism in obesity.J Clin Endocrinol Metab. 2011; 96: 1320-1326Crossref PubMed Scopus (91) Google Scholar]. Preexisting vitamin D deficiencies and elevated PTH levels in patients being evaluated for bariatric surgery have been found to be as high as 60%–84% and 42.2%–49%, respectively [6Carlin A.M. Rao D.S. Meslemani A.M. et al.Prevalence of vitamin D depletion among morbidly obese patients seeking gastric bypass surgery.Surg Obes Relat Dis. 2006; 2: 98-103Abstract Full Text Full Text PDF PubMed Scopus (130) Google Scholar, 7Fish E. Beverstein G. Olson D. Reinhardt S. Garren M. Gould J. Vitamin D status of morbidly obese bariatric surgery patients.J Surg Res. 2010; 164: 198-202Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar, 8Alexandrou A. Armeni E. Kaparos G. et al.Bsm1 vitamin D receptor polymorphism and calcium homeostasis following bariatric surgery.J Invest Surg. 2015; 28: 8-17Crossref PubMed Scopus (7) Google Scholar]. It has been identified that leptin, a hormone secreted by adipocytes which is increased in individuals with a higher fat mass, regulates bone mass directly and indirectly via PTH in animal models with leptin-deficient mice. Leptin increases cortical bone mass but may have an adverse effect on trabecular bone mass [[9]Savvidis C. Tournis S. Dede A.D. Obesity and bone metabolism.Hormones (Athens). 2018; 17: 205-217Crossref PubMed Scopus (66) Google Scholar]. Case control data suggest that leptin plays a role in elevating PTH levels. In patients with obesity, serum leptin levels were the highest predictive variable for an elevated serum PTH level. The mechanism is unknown, but it is theorized that leptin may increase parathyroid mass directly through a mitogenic effect [[5]Grethen E. McClintock R. Gupta C.E. et al.Vitamin D and hyperparathyroidism in obesity.J Clin Endocrinol Metab. 2011; 96: 1320-1326Crossref PubMed Scopus (91) Google Scholar]. Lower serum levels of vitamin D in patients with obesity can also be due to a dilutional effect of distribution into fat in these patients. In addition, patients with obesity typically need a higher dose of vitamin D replacement to achieve the same serum level as normal-weight patients. Because of the high prevalence of vitamin D deficiency and secondary hyperparathyroidism (despite normal calcium) in the obese population, obtaining a baseline preoperative assessment of bone health continues to remain standard. The specific recommendations remain unchanged from the prior statement, and consist of laboratory testing of 25-OHD, intact PTH levels, and serum alkaline phosphatase, as well as consideration of 24-hour urinary calcium in relationship to dietary intake, before bariatric surgery, with the initiation of treatment for deficiencies and documentation of improvement before surgery when possible. These recommendations are consistent with the ASMBS Integrated Health Nutritional Guidelines for the Surgical Weight Loss Patient 2016 [[10]Parrott J. Frank L. Rabena R. Craggs-Dino L. Isom K.A. Greiman L. American Society for Metabolic and Bariatric Surgery integrated health nutritional guidelines for the surgical weight loss patient 2016 update: micronutrients.Surg Obes Relat Dis. 2017; 13: 727-741Abstract Full Text Full Text PDF PubMed Scopus (349) Google Scholar]. A baseline dual-energy X-ray absorptiometry (DXA) scan is recommended by the National Osteoporosis Foundation Clinician’s Guide 2014 for all women aged 65 and older and men aged 70 and older. It is also recommended in postmenopausal women and men above age 50–69, based on the risk factor profile, and in men aged 50 and older who have had an adult age fracture, to diagnose and determine the degree of osteoporosis [[11]Cosman F. de Beur S.J. LeBoff M.S. et al.National Osteoporosis Foundation. Clinician's guide to prevention and treatment of osteoporosis.Osteoporos Int. 2014; 25: 2359-2381Crossref PubMed Scopus (1962) Google Scholar]. Preoperative DXA can also be considered in estrogen-deficient women and in premenopausal women and men who have risk factors or conditions associated with bone loss or low bone mass, to establish a baseline before bariatric surgery. There remain insufficient data to C. Brethauer S. et guidelines for the and of patients bariatric update: by American of Clinical of The Obesity American Society for Metabolic Bariatric Obesity and American Society of 25: Google Scholar]. the statement, has as a to BMD that may be more than DXA in patients with obesity. is to and tissue changes than DXA et loss after bariatric DXA and bone Res. 2014; PubMed Scopus Google Scholar]. It is also of changes of bone S.J. loss after bariatric and 2014; 2: Full Text Full Text PDF PubMed Scopus Google Scholar]. and DXA were found to the of patients who gastric bypass et loss after bariatric DXA and bone Res. 2014; PubMed Scopus Google Scholar]. in a of 24 patients DXA the and a of these same patients no in the bone or bone density the and in a of patients bariatric surgery found cortical bone loss, but trabecular bone increases and these were by a in PTH levels. were most in S.J. loss after bariatric and 2014; 2: Full Text Full Text PDF PubMed Scopus Google Scholar]. in patients that bone and bone the and were unchanged after surgery of bariatric bone loss, potential and Obes Metab. 2014; PubMed Scopus Google Scholar]. for in to DXA are and high obesity and of in guidelines from the American of of on the for the of Scholar]. The of over DXA higher of and a higher the and with has become loss when there is a of bone to and changes in that with bariatric procedures, as well as procedures, as for can to bone loss D. C. et metabolic and increased risk for after Int. Google Scholar]. the of bariatric surgery on bone metabolism and bone health to be and to the degree of weight loss are the potential for micronutrient deficiency and bypass in of and of gastric and may have a risk of micronutrient deficiency than the gastric or procedures. The of a bypass with as in with and procedures, may in additional to bone health. changes in as and are found after and these changes are to of the metabolic benefits of bariatric surgery, may also to bone it remains to levels of vitamin and parathyroid hormone before and in the after bariatric surgery C. R. et vitamin D and bone mineral density in women after obesity surgery.Obes Surg. PubMed Scopus Google Scholar, M. E. E. of gastric bypass on bone mineral parathyroid hormone and vitamin Surg. PubMed Scopus Google Scholar, V. M. et in bone metabolism after bariatric surgery by gastric bypass or 2017; PubMed Scopus Google Scholar, A. M. of gastric bypass and on bone mineral density and adipose 2017; PubMed Scopus Google Scholar, A. Vitamin D deficiency and increase in gastric bypass in 2018; PubMed Scopus Google Scholar]. loss after is to that of changes that can with weight loss or procedures, as the and is to any additional micronutrient M. D. of on bone and mineral metabolism in obese Surg. PubMed Scopus Google Scholar, E. G. G. C. R. of weight loss on bone of and Surg. 13: PubMed Scopus Google Scholar, J.M. J. metabolism in obese patients following Surg. 2008; 18: PubMed Scopus Google Scholar]. It continues to be that can in calcium deficiency and metabolic bone with of has been to decreased dietary calcium decreased due to the calcium is decreased secondary to gastric of vitamin and decreased mechanical on [[1]Kim J. Brethauer S. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee, position statement. Metabolic bone changes after bariatric surgery.Surg Obes Relat Dis. 2015; 11: 406-411Abstract Full Text Full Text PDF PubMed Scopus (41) Google C.M. et calcium after gastric bypass surgery of vitamin D Res. 2015; PubMed Scopus Google G. and mineral metabolism in patients gastric Int. 2014; 25: PubMed Scopus Google Scholar]. patients with obesity have a high prevalence of vitamin D deficiency baseline and the prevalence may over A. Vitamin D deficiency and increase in gastric bypass in 2018; PubMed Scopus Google Scholar]. In addition, rates of secondary hyperparathyroidism are high in patients than in patients secondary hyperparathyroidism may in patients normal levels of calcium and vitamin as calcium and may a role C. R. et vitamin D and bone mineral density in women after obesity surgery.Obes Surg. PubMed Scopus Google J. C. The of bariatric surgery on bone and PubMed Scopus Google de et and bone health in women after bariatric surgery a in de Surg. PubMed Scopus Google Scholar]. factor is decreased mechanical to weight loss after that mechanical normal is the mechanism in bone mass, and A evaluated bone loss after be or decreased by the study had patient and a of the that with patients were to the loss of as the of the and with of bone et bone loss in women with severe obesity after gastric a Clin Endocrinol Metab. PubMed Scopus Google Scholar]. In addition, changes in that are in fat as leptin, and are after there are increases in and which has been in to increase this has been in patients BMD and DXA J. C. The of bariatric surgery on bone and PubMed Scopus Google The of bariatric surgery on bone Clin 2017; Full Text Full Text PDF PubMed Scopus Google Scholar]. in to to of of bone remodeling, as of of weight loss or and this be to the increased levels of after M. et of gastric bypass and gastric on bone in obese patients with Clin Endocrinol Metab. PubMed Scopus Google Scholar]. can be for decreased BMD after as patients may than recommended M. of in bone mass after bariatric PubMed Scopus Google Scholar]. patients higher bone turnover, more and BMD in the and than patients who weight after or D. J. R. et following weight loss surgery is associated with treatment and changes in secreted PubMed Scopus Google L. et effect of a and on the and bone mass of obese patients who have gastric bypass surgery.Obes Surg. 2017; PubMed Scopus Google Scholar]. of bone can be to bone in as increased bone has been to as as after surgery and may be for A. Center Bariatric surgery, bone loss, obesity and PubMed Scopus Google Scholar]. alkaline phosphatase, and are of and bone et loss after bariatric DXA and bone Res. 2014; PubMed Scopus Google of gastric bypass on bone mineral density and of bone Obes Relat Dis. 2014; Full Text Full Text PDF PubMed Scopus Google Scholar]. and have been as for bone to weight after bariatric surgery of bariatric bone loss, potential and Obes Metab. 2014; PubMed Scopus Google Scholar]. is that bone and has been to be increased after and C. R. C. et levels and changes in bone metabolism after bariatric surgery.J Clin Endocrinol Metab. 2015; PubMed Scopus Google Scholar]. continue to that bone increases after with increases in and et loss after bariatric DXA and bone Res. 2014; PubMed Scopus Google of bariatric bone loss, potential and Obes Metab. 2014; PubMed Scopus Google of gastric bypass on bone mineral density and of bone Obes Relat Dis. 2014; Full Text Full Text PDF PubMed Scopus Google E. A. M. et mineral density and of vitamin D calcium in the after bariatric Surg. 2014; PubMed Scopus Google Scholar]. The increases in bone are and to the increases in bone have been S.J. loss after bariatric and 2014; 2: Full Text Full Text PDF PubMed Scopus Google Scholar]. It is the increase in bone is an adverse effect of the surgery or a to the weight loss and A. Center Bariatric surgery, bone loss, obesity and PubMed Scopus Google Scholar]. the last statement, there has been a continued increase in the of with a in the of to weight loss and continued the with bone loss is as by elevated of bone [[9]Savvidis C. Tournis S. Dede A.D. Obesity and bone metabolism.Hormones (Athens). 2018; 17: 205-217Crossref PubMed Scopus (66) Google A. M. of gastric bypass and on bone mineral density and adipose 2017; PubMed Scopus Google Scholar]. et N. L. bone in patients to bariatric surgery 2018; Full Text Full Text PDF PubMed Scopus Google levels of and patients with who and patients with who a levels were increased by an of and levels by an of from baseline in with and for patients in the N. L. bone in patients to bariatric surgery 2018; Full Text Full Text PDF PubMed Scopus Google Scholar]. The to be associated with bone loss after are and to those following The mechanical of the in also for [[9]Savvidis C. Tournis S. Dede A.D. Obesity and bone metabolism.Hormones (Athens). 2018; 17: 205-217Crossref PubMed Scopus (66) Google Scholar]. to a in BMD loss the and than the The of bariatric surgery on bone Clin 2017; Full Text Full Text PDF PubMed Scopus Google Scholar]. there is an in intake, as well as decreased and gastric to the decreased and of calcium N. de C. et of bariatric surgery on bone mineral of gastric bypass and Surg. PubMed Scopus Google Scholar]. have and in of et N. L. bone in patients to bariatric surgery 2018; Full Text Full Text PDF PubMed Scopus Google on patients who and DXA the and and a of In that bone of the and the with patients who found that the of BMD loss N. L. bone in patients to bariatric surgery 2018; Full Text Full Text PDF PubMed Scopus Google Scholar]. et A. M. of gastric bypass and on bone mineral density and adipose 2017; PubMed Scopus Google patients and patients after surgery and found a BMD the and in with patients on a DXA scan but on that the changes were have also BMD loss among and V. M. et in bone metabolism after bariatric surgery by gastric bypass or 2017; PubMed Scopus Google N. de C. et of bariatric surgery on bone mineral of gastric bypass and Surg. PubMed Scopus Google including a by et J. in bone metabolism after gastric a Surg. PubMed Scopus Google that and found that the had levels of interval to and calcium to as well as higher levels of PTH and the mass changes and BMD by DXA or were in In et C.M. A. A study of the in bone mineral density after bariatric Obes Relat Dis. 2015; 11: Full Text Full Text PDF PubMed Scopus Google a study and in patients and baseline and DXA The BMD the were in the and the but the BMD loss the higher in the C.M. A. A study of the in bone mineral density after bariatric Obes Relat Dis. 2015; 11: Full Text Full Text PDF PubMed Scopus Google Scholar]. have found a in BMD the and levels but the M. et size, bone mineral and in obese women after a Res. 2015; PubMed Scopus Google found a in BMD all levels following M. L. V. mineral changes in and in obese women after a Surg. PubMed Scopus Google Scholar]. have an increase in BMD the level after J. et and changes in bone mineral density after Surg. PubMed Scopus Google Scholar]. Vitamin D deficiency and with secondary as with has been as to the BMD In the after Bariatric Surgery et C. R. C. et levels and changes in bone metabolism after bariatric surgery.J Clin Endocrinol Metab. 2015; PubMed Scopus Google patients who had or and an and a with for a of 24 The vitamin D and vitamin and supplementation with and with a which of the The study found in of bone levels of of BMD the and and BMD in the with the control Weight loss in to the had a in C. R. C. et levels and changes in bone metabolism after bariatric surgery.J Clin Endocrinol Metab. 2015; PubMed Scopus Google Scholar]. bone loss as with has also been after by N. de C. et of bariatric surgery on bone mineral of gastric bypass and Surg. PubMed Scopus Google F. et in bone mineral density after or gastric with variations in vitamin and Surg. 2014; PubMed Scopus (71) Google et on bone density and in patients with to bariatric surgery 2015; PubMed Scopus Google Scholar]. Despite the of evidence to bone loss after and there are of the are than with There is variable regarding baseline and vitamin deficiencies and also DXA to BMD loss, has been to be more in patients with higher as well as more following weight loss The of bariatric surgery on bone Clin 2017; Full Text Full Text PDF PubMed Scopus Google Scholar]. there is evidence to suggest that BMD loss after to a degree as after and should continue to be are to the the BMD after may be associated with of vitamin D deficiency and secondary hyperparathyroidism to secondary to serum is a of severe after and may also bone loss in these individuals S. S. et bone after Surg. PubMed Scopus Google Scholar]. In the interval et V. et parathyroid hormone and 25-hydroxyvitamin D before and after Surg. 2018; 28: PubMed Scopus Google the of calcium and vitamin D deficiencies and secondary hyperparathyroidism over a interval in a of over and preoperative and including in which is after or The prevalence of vitamin D deficiency decreased to after surgery baseline to after The prevalence of hyperparathyroidism before surgery and increased after surgery, the prevalence of and the prevalence increased after to V. et parathyroid hormone and 25-hydroxyvitamin D before and after Surg. 2018; 28: PubMed Scopus Google Scholar]. loss, has also been after after and normal levels of vitamin D and Despite the changes that in bone metabolism after bariatric surgery, published have to a increased risk after bariatric surgery [[1]Kim J. Brethauer S. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee. American Society for Metabolic and Bariatric Surgery Clinical Issues Committee, position statement. Metabolic bone changes after bariatric surgery.Surg Obes Relat Dis. 2015; 11: 406-411Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar]. The available interval evidence remains and of with a of men and postmenopausal with and limited data from treatment with bariatric surgery. Despite there to be a interval of data to an increased risk after bariatric surgery, with the risk in than in and the risk in than in and A from 2016 that with surgical patients and control with from to no in bone density the It a in bone density the which in patients who had surgery et bariatric surgery and bone mineral a Surg. PubMed Scopus Google Scholar]. The BMD the as well as the has been found to in patients in M. of in bone mass after bariatric PubMed Scopus Google Scholar]. A study from that the risk of after higher than in the population, and the risk as high as in patients over a and over of these were et risk following bariatric a Int. 2014; 25: PubMed Scopus Google Scholar]. In addition, in a study with patients who had had a higher risk of as with patients who had and the higher risk for surgery risk after bariatric gastric bypass gastric Res. 2017; PubMed Scopus Google Scholar]. In a study from the United evaluated more than patients with obesity who were for a and found no increases in the of in and J. C. The of bariatric surgery on bone and PubMed Scopus Google The of bariatric surgery on bone Clin 2017; Full Text Full Text PDF PubMed Scopus Google Scholar]. the Surgical and in which patients with were to and that the of higher bone density loss in the surgical and were in and patients. were in and patients et on bone density and in patients with to bariatric surgery 2015; PubMed Scopus Google et Bariatric surgery for 2014; PubMed Scopus Google Scholar]. A study from the Integrated more than patients after bariatric surgery, including and and with a control for sex, and who were for study that patients bariatric surgery were more to than were obese and The risk higher in the bariatric than in the obese and surgery, the of from that of obesity to a for with the risk of a decreased the increased for and or but for C. S. et in risk and after bariatric PubMed Scopus Google Scholar]. study from the National in patients against in a a increased risk for any after in patients with and a increased risk in control patients the also an increased risk of after surgery as a factor to risk M. et risk after gastric bypass a Res. 2018; PubMed Scopus (71) Google Scholar]. A in from the Obesity weight patients with patients. The weight loss and The for were than study patients in the had higher of all and with and weight patients and this study data on patients and S. M. et risk after bariatric surgery in obese to of a PubMed Scopus Google Scholar]. and the highest increased risk after bariatric surgery has been after with obese the risk increased by after C. S. et in risk and after bariatric PubMed Scopus Google Scholar]. In a study from the National Health of surgery patients were to obese there a increased risk of in the surgical but a after et risk after bariatric a 2015; PubMed Scopus Google Scholar]. by gastric for calcium in an based on review have that BMD monitoring, and has been associated with of micronutrient or decreased BMD D. et of of an review and 2017; PubMed Scopus Google E. et gastric calcium in a Res. 2010; 25: PubMed Scopus Google Scholar]. The and a on in for an increased risk associated with these in when data available and on the increased risk of of the and with the of and Scholar]. of or has been found to increase the In patients older than 50 a study from that the risk increases with the of as well as the dose S. and risk of 2006; PubMed Scopus Google Scholar]. A from with over The from this study increased of and in patients to a increase in the risk in to study S. S. A. and risk of a review and of 2011; PubMed Scopus Google Scholar]. there is in the evidence for the risk of fracture, in patients who are an older age and on has a level of to BMD monitoring in patients on risk factors for osteoporosis The and benefits of of expert review and from the American 2017; Full Text Full Text PDF PubMed Scopus Google Scholar]. is associated with vitamin and mineral deficiencies in bone which may the of bone on the of degree of weight loss, nutritional intake, with sex, race, and of any additional risk as or preoperative for the of vitamin D deficiency and with treatment is recommended for all and of bone is recommended for all with specific recommendations to be a interval of data to increased after bariatric surgery, with the risk in than in and the risk in than in and as well as are to the the and determine monitoring and is to calcium due to in the or of gastric [[10]Parrott J. Frank L. Rabena R. Craggs-Dino L. Isom K.A. Greiman L. American Society for Metabolic and Bariatric Surgery integrated health nutritional guidelines for the surgical weight loss patient 2016 update: micronutrients.Surg Obes Relat Dis. 2017; 13: 727-741Abstract Full Text Full Text PDF PubMed Scopus (349) Google C. Brethauer S. et guidelines for the and of patients bariatric update: by American of Clinical of The Obesity American Society for Metabolic Bariatric Obesity and American Society of 25: Google Scholar].

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