Abstract
Purpose
Metabolic surgery and lifestyle intervention are two common methods used to treat obesity, but the effects of weight loss on bone mineral density (BMD) remain controversial. Our aim was to evaluate changes in BMD of the total hip, femoral neck, and lumbar spine after weight loss caused by metabolic surgery or lifestyle intervention.
Materials and Methods
We searched PubMed, Web of Science, and the Cochrane Library to identify relevant studies published before 5 August 2020. The primary outcomes, including the BMD of the total hip, femoral neck, and lumbar spine before and 12 months after metabolic surgery or lifestyle intervention, were extracted.
Results
A total of 19 studies with 1095 participants with obesity were included. Among them, 603 participants with obesity accepted metabolic surgery, while 492 accepted lifestyle intervention. At 12 months after weight loss, the BMD of the total hip decreased significantly in obese patients (mean difference [MD] = 0.06 g/cm2; 95% confidence interval [CI] 0.03 to 0.08; I2 = 67%; P < 0.001), while the BMD of the lumbar spine did not significantly change (P > 0.05). In the subgroup analysis, the BMD of the femoral neck decreased significantly at 12 months in obese patients who underwent metabolic surgery (MD = 0.08 g/cm2; 95% CI 0.04 to 0.13; I2 = 84%; P < 0.001), while it did not significantly change in obese patients who underwent lifestyle treatment (P > 0.05).
Conclusion
Regardless of whether the patients underwent metabolic surgery or lifestyle treatment, the BMD of the total hip significantly decreased in obese patients after weight loss. Different methods used to lose weight may have different effects on the BMD of the femoral neck. Prospective studies, preferably randomized controlled trials (RCTs), are still required to investigate whether the effects of the two treatments on bone metabolism are truly different.
Similar content being viewed by others
References
NCD-RisC NRFC. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19·2 million participants. Lancet. 2016;387:1377–96.
Ryan D, Heaner M. Guidelines (2013) for managing overweight and obesity in adults. Preface to the full report. Obesity (Silver Spring) 2014;22 Suppl 2:S1-S3
Muller-Stich BP, Senft JD, Warschkow R, et al. Surgical versus medical treatment of type 2 diabetes mellitus in nonseverely obese patients: a systematic review and meta-analysis. Ann Surg. 2015;261:421–9.
Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016;39:861–77.
Nguyen T, Sambrook P, Kelly P, et al. Prediction of osteoporotic fractures by postural instability and bone density. BMJ. 1993;307:1111–5.
Grethen E, Hill KM, Jones R, et al. Serum leptin, parathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012;97:1655–62.
Yang S, Shen X. Association and relative importance of multiple obesity measures with bone mineral density: the National Health and Nutrition Examination Survey 2005-2006. Arch Osteoporos. 2015;10:14.
Zhu K, Hunter M, James A, et al. Associations between body mass index, lean and fat body mass and bone mineral density in middle-aged Australians: the Busselton Healthy Ageing Study. Bone. 2015;74:146–52.
Compston JE, Watts NB, Chapurlat R, et al. Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med. 2011;124:1043–50.
Ko B, Myung SK, Cho K, et al. Relationship between bariatric surgery and bone mineral density: a meta-analysis. Obes Surg. 2016;26:1414–21.
Adamczyk P, Buzga M, Holeczy P, et al. Bone mineral density and body composition after laparoscopic sleeve gastrectomy in men: a short-term longitudinal study. Int J Surg. 2015;23:101–7.
Zibellini J, Seimon RV, Lee CM, et al. Does diet-induced weight loss Lead to bone loss in overweight or obese adults? A systematic review and meta-analysis of clinical trials. J Bone Miner Res. 2015;30:2168–78.
Hinton PS, Rector RS, Donnelly JE, et al. Total body bone mineral content and density during weight loss and maintenance on a low- or recommended-dairy weight-maintenance diet in obese men and women. Eur J Clin Nutr. 2010;64:392–9.
Ruiz-Tovar J, Oller I, Priego P, et al. Short- and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23:861–6.
Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med. 2009;151:W65–94.
Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.
Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5.
Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.
Guerrero-Perez F, Casajoana A, Gomez-Vaquero C, et al. Changes in bone mineral density in patients with type 2 diabetes after different bariatric surgery procedures and the role of gastrointestinal hormones. Obes Surg. 2020;30:180–8.
Luhrs AR, Davalos G, Lerebours R, et al. Determining changes in bone metabolism after bariatric surgery in postmenopausal women. Surg Endosc. 2020;34:1754–60.
Sukumar D, Ambia-Sobhan H, Zurfluh R, et al. Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: a randomized, controlled trial. J Bone Miner Res. 2011;26:1339–48.
Seimon RV, Wild-Taylor AL, Keating SE, et al. Effect of weight loss via severe vs moderate energy restriction on lean mass and body composition among postmenopausal women with obesity: the TEMPO diet randomized clinical trial. JAMA Netw Open. 2019;2:e1913733.
Foster GD, Wyatt HR, Hill JO, et al. Weight and metabolic outcomes after 2 years on a low-carbohydrate versus low-fat diet: a randomized trial. Ann Intern Med. 2010;153:147–57.
Villareal DT, Chode S, Parimi N, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med. 2011;364:1218–29.
Carrasco F, Basfi-Fer K, Rojas P, et al. Calcium absorption may be affected after either sleeve gastrectomy or Roux-en-Y gastric bypass in premenopausal women: a 2-y prospective study. Am J Clin Nutr. 2018;108:24–32.
Hsin MC, Huang CK, Tai CM, et al. A case-matched study of the differences in bone mineral density 1 year after 3 different bariatric procedures. Surg Obes Relat Dis. 2015;11:181–5.
Tan HC, Tan MZ, Tham KW, et al. One year changes in QCT and DXA bone densities following bariatric surgery in a multiethnic Asian cohort. Osteoporos Sarcopenia. 2015;1:115–20.
Blom-Hogestol IK, Mala T, Kristinsson JA, et al. Changes in bone quality after Roux-en-Y gastric bypass: a prospective cohort study in subjects with and without type 2 diabetes. Bone. 2020;130:115069.
Guerrero-Pérez F, Casajoana A, Gómez-Vaquero C, et al. Long-term effects in bone mineral density after different bariatric procedures in patients with type 2 diabetes: outcomes of a randomized clinical trial. J Clin Med. 2020;9:1830.
Frederiksen KD, Hanson S, Hansen S, et al. Bone structural changes and estimated strength after gastric bypass surgery evaluated by HR-pQCT. Calcif Tissue Int. 2016;98:253–62.
Luger M, Kruschitz R, Winzer E, et al. Changes in bone mineral density following weight loss induced by one-anastomosis gastric bypass in patients with vitamin D supplementation. Obes Surg. 2018;28:3454–65.
Casagrande DS, Repetto G, Mottin CC, et al. Changes in bone mineral density in women following 1-year gastric bypass surgery. Obes Surg. 2012;22:1287–92.
Raoof M, Näslund I, Rask E, et al. Effect of gastric bypass on bone mineral density, parathyroid hormone and vitamin D: 5 years follow-up. Obes Surg. 2016;26:1141–5.
Obinwanne KM, Riess KP, Kallies KJ, et al. 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.
Geoffroy M, Charlot-Lambrecht I, Chrusciel J, et al. Impact of bariatric surgery on bone mineral density: observational study of 110 patients followed up in a specialized center for the treatment of obesity in France. Obes Surg. 2019;29:1765–72.
Giusti V, Gasteyger C, Suter M, et al. Gastric banding induces negative bone remodelling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obes. 2005;29:1429–35.
Arnold M, Pandeya N, Byrnes G, et al. Global burden of cancer attributable to high body-mass index in 2012: a population-based study. Lancet Oncol. 2015;16:36–46.
Li S, Xiao J, Ji L, et al. BMI and waist circumference are associated with impaired glucose metabolism and type 2 diabetes in normal weight Chinese adults. J Diabetes Complicat. 2014;28:470–6.
Ablett AD, Boyle BR, Avenell A. Fractures in adults after weight loss from bariatric surgery and weight management programs for obesity: systematic review and meta-analysis. Obes Surg. 2019;29:1327–42.
Yu EW, Kim SC, Sturgeon DJ, et al. Fracture risk after Roux-en-Y gastric bypass vs adjustable gastric banding among Medicare beneficiaries. JAMA Surg. 2019;154:746–53.
Johansson H, Kanis JA, Oden A, et al. A meta-analysis of the association of fracture risk and body mass index in women. J Bone Miner Res. 2014;29:223–33.
Masud T, Langley S, Wiltshire P, et al. Effect of spinal osteophytosis on bone mineral density measurements in vertebral osteoporosis. BMJ. 1993;307:172–3.
Johnell O, Kanis JA, Oden A, et al. Predictive value of BMD for hip and other fractures. J Bone Miner Res. 2005;20:1185–94.
Lang T, LeBlanc A, Evans H, et al. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res. 2004;19:1006–12.
Kazakia GJ, Tjong W, Nirody JA, et al. The influence of disuse on bone microstructure and mechanics assessed by HR-pQCT. Bone. 2014;63:132–40.
Li X, Zhang Y, Kang H, et al. Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem. 2005;280:19883–7.
Luo XH, Guo LJ, Xie H, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res. 2006;21:1648–56.
Lenchik L, Register TC, Hsu FC, et al. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone. 2003;33:646–51.
Blain H, Vuillemin A, Guillemin F, et al. Serum leptin level is a predictor of bone mineral density in postmenopausal women. J Clin Endocrinol Metab. 2002;87:1030–5.
Ma W, Huang T, Zheng Y, et al. Weight-loss diets, adiponectin, and changes in cardiometabolic risk in the 2-year POUNDS lost trial. J Clin Endocrinol Metab. 2016;101:2415–22.
Abbenhardt C, McTiernan A, Alfano CM, et al. Effects of individual and combined dietary weight loss and exercise interventions in postmenopausal women on adiponectin and leptin levels. J Intern Med. 2013;274:163–75.
Cifuentes M, Riedt CS, Brolin RE, et al. Weight loss and calcium intake influence calcium absorption in overweight postmenopausal women. Am J Clin Nutr. 2004;80:123–30.
Shapses SA, Sukumar D, Schneider SH, et al. Vitamin D supplementation and calcium absorption during caloric restriction: a randomized double-blind trial. Am J Clin Nutr. 2013;97:637–45.
Devlin MJ, Cloutier AM, Thomas NA, et al. Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res. 2010;25:2078–88.
Kim TY, Schwartz AV, Li X, et al. Bone marrow fat changes after gastric bypass surgery are associated with loss of bone mass. J Bone Miner Res. 2017;32:2239–47.
Cosman F, de Beur SJ, LeBoff MS, et al. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25:2359–81.
Campanha-Versiani L, Pereira D, Ribeiro-Samora GA, et al. The effect of a muscle weight-bearing and aerobic exercise program on the body composition, muscular strength, biochemical markers, and bone mass of obese patients who have undergone gastric bypass surgery. Obes Surg. 2017;27:2129–37.
Funding
This work was supported by the National Key R&D Program of China (2016YFC1305000, 2016YFC1305001), the National Natural Science Foundation of China (91749118, 81770775), the Science and Technology Major Project of Hunan Province (2017SK1020), and the Planned Science and Technology Project of Hunan Province (2017RS3015).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval
For this type of study, formal consent is not required.
Informed Consent Statement
Does not apply.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 91 kb)
Rights and permissions
About this article
Cite this article
Chen, X., Zhang, J. & Zhou, Z. Changes in Bone Mineral Density After Weight Loss Due to Metabolic Surgery or Lifestyle Intervention in Obese Patients. OBES SURG 31, 1147–1157 (2021). https://doi.org/10.1007/s11695-020-05095-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11695-020-05095-x