Bariatric surgery, bone loss, obesity and possible mechanisms
Abstract
Summary: Bariatric surgery remains the most effective treatment for severely obese patients. However, the potential long‐term effects of bariatric surgical procedures on health, including bone health, are only partially understood. The goal of this review was to present data on the impact of bariatric surgery on bone metabolism and to analyse possible reasons for the loss of bone mass that frequently occurs after bariatric surgery. Such factors include nutritional deficiencies, rapid weight loss per se, effects of fat‐derived adipokines and gut‐derived appetite‐regulatory hormones. However, the relative roles of these factors in skeletal regulation and the mechanisms by which they work are not yet fully defined. Our review was focussed on the complex relationship between body weight, fat mass and bone mass, as well as peripheral and central mediators potentially involved in the dual regulation of both energy and bone homeostasis. We also review the data on the inverse relationship between central obesity, bone marrow fat and osteoporosis. As the number of bariatric operations increases, it is imperative to recognize mechanisms responsible for bariatric surgery‐induced bone loss, with careful monitoring of bone health including long‐term fracture incidence in patients undergoing these procedures.
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Sleeve gastrectomy produces weight loss between that of purely restrictive and malabsorptive procedures.
“Sleeve gastrectomy is becoming increasingly common, with weight loss falling between the purely restrictive and malabsorptive procedures (1 to 2 year weight loss: 20-30%; excess BMI loss: 45-80%).36, 46-50.”
From Bone loss after bariatric surgery: causes, consequences, and management (2014) · cites this paper as [50]
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Ghrelin and Bone: Is There an Association in Older Adults?: The Rancho Bernardo Study
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Carine Chavey, A., Boucher, J., Monthouel, M.-N., Sage, E. H., Castan‐Laurell, I., Valet, P., Tartare‐Deckert, S., & OBBERGHEN, E. V. (2006) · Obesity · doi:10.1038/oby.2006.220 · Cited by 45 · see citing works
Simulated Change in Body Fatness Affects Hologic QDR 4500A Whole Body and Central DXA Bone Measures
Evans, E. M., Mojtahedi, M. C., Kessinger, R. B., & Misic, M. M. (2006) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2006.04.117 · Cited by 42 · see citing works
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Solutions in weight control: lessons from gastric surgery
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Trabecular bone structure in patients with primary hyperparathyroidism
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Evidence for the Involvement of Resistin in Inflammation and Cardiovascular Disease
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Impact of Gastric Banding on Plasma Ghrelin, Growth Hormone, Cortisol, DHEA and DHEA-S Levels
Ram, E., Vishne, T. H., Diker, D., Gal-Ad, I., Maayan, R., Lerner, I., Dreznik, Z., Seror, D., Vardi, P., & Weizman, A. (2005) · Obesity Surgery · doi:10.1381/0960892055002329 · Cited by 36 · see citing works
Serum peptide YY in response to short-term overfeeding in young men
Cahill, F., Shea, J. L., Randell, E. W., Vasdev, S., & Sun, G. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.003624 · Cited by 34 · see citing works
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Central regulation of bone mass
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Osteopenia in genetically diabetic db/db mice and effects of 1α-hydroxyvitamin D3 on the osteopenia
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Expression of ghrelin in fundus is increased after gastric banding in morbidly obese patients
Uzzan, B., Catheline, J.-M., Lagorce, C., Airinei, G., Bon, C., Cohen, R., Perret, G. Y., Aparicio, T., & Benamouzig, R. (2007) · Obesity Surgery · doi:10.1007/s11695-007-9197-9 · Cited by 24 · see citing works
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Lingvay, I., Cohen, R. V., Roux, C. W. L., & Sumithran, P. (2024) · The Lancet · doi:10.1016/s0140-6736(24)01210-8 · Cited by 433 · see citing works
Review article: the nutritional and pharmacological consequences of obesity surgery
Stein, J. M., Stier, C. K., Raab, H., & Weiner, R. A. (2014) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12872 · Cited by 257 · see citing works
Effects of the gut microbiota on bone mass
Ohlsson, C., & Sjögren, K. (2014) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2014.11.004 · Cited by 235 · see citing works
Obesity in CKD--what should nephrologists know?
Stenvinkel, P., Zoccali, C., & Ikizler, T. (2013) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013040330 · Cited by 205 · see citing works
Bone Metabolism After Bariatric Surgery
Yu, E. W.-Y. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2226 · Cited by 212 · see citing works
Bone loss after bariatric surgery: causes, consequences, and management
Stein, E. M., & Silverberg, S. J. (2014) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70183-9 · Cited by 199 · see citing works
BMI and BMD: the potential interplay between obesity and bone fragility
Palermo, A., Tuccinardi, D., Defeudis, G., Watanabe, M., D’Onofrio, L., Lauria Pantano, A., Napoli, N., Pozzilli, P., & Manfrini, S. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph13060544 · Cited by 197 · see citing works
Bone Health After Bariatric Surgery
Gagnon, C., & Schafer, A. L. (2018) · JBMR Plus · doi:10.1002/jbm4.10048 · Cited by 177 · see citing works
Obesity and hypovitaminosis D: causality or casualty?
Migliaccio, S., Nisio, A. D., Mele, C., Scappaticcio, L., Savastano, S., & Colao, A. (2019) · International Journal of Obesity Supplements · doi:10.1038/s41367-019-0010-8 · Cited by 198 · see citing works
Zibellini, J., Seimon, R. V., Lee, C. M., Gibson, A. A., Hsu, M. S., Shapses, S. A., Nguyen, T. V., & Sainsbury, A. (2015) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2564 · Cited by 157 · see citing works
“Whether or not obesity per se has an effect on fracture risk, emerging evidence suggests that obesity treatment, namely bariatric surgery—which induces weight losses of up to 75% of excess body weight that are maintained for up to 10 to 14 years postsurgery((13))—results in bone loss.((14,15)) However dietinduced weig…”
BackgroundSelf-citationBone Loss After Bariatric Surgery: Discordant Results Between DXA and QCT Bone Density
Yu, E. W.-Y., Bouxsein, M., Roy, A. E., Baldwin, C. M., Cange, A., Neer, R. M., Kaplan, L. M., & Finkelstein, J. S. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2063 · Cited by 153 · see citing works
“Gastric bypass surgery is accompanied by a variety of changes in the gastrointestinal, fat‐related, and inflammatory hormones, some of which may have direct skeletal effects.((20)) Further studies are needed to determine whether postsurgical changes to hormonal profiles may potentially be associated with skeletal chan…”
BackgroundFracture Risk After Bariatric Surgery
Lu, C., Chang, Y., Chang, H., Kuo, C.-S., Huang, C.-T., Hsu, C., & Huang, K. (2015) · Medicine · doi:10.1097/md.0000000000002087 · Cited by 153 · see citing works
Two-Year Changes in Bone Density After Roux-en-Y Gastric Bypass Surgery
Yu, E. W.-Y., Bouxsein, M., Putman, M. S., Monis, E. L., Roy, A. E., Pratt, J. S. A., Butsch, W. S., & Finkelstein, J. S. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-4341 · Cited by 148 · see citing works
“Gastric bypass surgery is accompanied by large changes in gastrointestinal, adipocytic, and neuroendocrine hormones, many of which are postulated to have direct or indirect effects on the skeleton (29, 30).”
BackgroundChanges in Skeletal Integrity and Marrow Adiposity during High-Fat Diet and after Weight Loss
Scheller, E. L., Khoury, B. M., Moller, K. L., Wee, N. K. Y., Khandaker, S., Kozloff, K. M., Abrishami, S., Zamarron, B. F., & Singer, K. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00102 · Cited by 131 · see citing works
“Surgical interventions of bariatric surgery (Roux-en Y gastric bypass, laparoscopic adjustable gastric banding, and sleeve gastrectomy) have all been associated with a decline in bone mass despite improvements in metabolic health (32).”
BackgroundFracture Risk After Bariatric Surgery: Roux‐en‐Y Gastric Bypass Versus Adjustable Gastric Banding
Yu, E. W.-Y., Lee, M. P., Landon, J. E., Lindeman, K. G., & Kim, S. C. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3101 · Cited by 123 · see citing works
“It is possible that other hormonal changes in RYGB, such as changes in gastrointestinal or adipocytic hormones, may be directly responsible for the bone loss that accompanies this procedure.((45,46)) Alternatively, it has been suggested that RYGB patients experience an increased risk of falls,((35,47)) which might con…”
BackgroundChanges in bone metabolism after bariatric surgery by gastric bypass or sleeve gastrectomy
Ivaska, K. K., Huovinen, V., Soinio, M., Hannukainen, J. C., Saunavaara, V., Salminen, P. T. P., Helmiö, M., Parkkola, R. K., Nuutila, P., & Kiviranta, R. (2016) · Bone · doi:10.1016/j.bone.2016.11.001 · Cited by 106 · see citing works
Homan, J., Betzel, B., Aarts, E. O., Doğan, K., van Laarhoven, K. J. H. M., Janssen, I. M. C., & Berends, F. J. (2015) · Obesity Surgery · doi:10.1007/s11695-015-1570-5 · Cited by 105 · see citing works
“When deficiencies for calcium and vitamin D are not corrected or treated adequately, these patients are at risk of developing early osteoporosis [20], which is, unfortunately, irreversible.”
BackgroundFernando Carrasco, N., Basfi-fer, K., Rojas, P., Valencia, A., Csendes, A., Codoceo, J., Inostroza, J., & Manuel Ruz, O. (2014) · Obesity Surgery · doi:10.1007/s11695-014-1179-0 · Cited by 104 · see citing works
“However, the reduction in plasma ghrelin concentration observed after SG could be related to increased bone loss [36].”
BackgroundLindeman, K. G., Greenblatt, L. B., Rourke, C., Bouxsein, M., Finkelstein, J. S., & Yu, E. W.-Y. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01496 · Cited by 103 · see citing works
Paccou, J., Martignène, N., Lespessailles, É., Babykina, E., Pattou, F. N., Cortet, B., & Ficheur, G. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4012 · Cited by 103 · see citing works
Fibroblast growth factor 21 night watch: advances and uncertainties in the field
Kharitonenkov, A., & DiMarchi, R. D. (2016) · Journal of Internal Medicine · doi:10.1111/joim.12580 · Cited by 97 · see citing works
Schafer, A. L., Kazakia, G. J., Vittinghoff, E., Stewart, L., Rogers, S. J., Kim, T. Y., Carter, J. T., Posselt, A. M., Pasco, C., Shoback, D., et al. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3371 · Cited by 99 · see citing works
“41) P1NP (ng/mL) 32 (26, 47) 32 (26, 44) 45 (23, 56) 39 (28, 48) BAP (mg/L) 13 (10, 18) 12 (9, 17) 19 (11, 25) 13 (13, 15) OC (ng/mL) 11 (8, 14) 11 (8, 13) 12 (8, 17) 10 (8, 18) Areal BMD (DXA) (g/cm(2)) Femoral neck 0.”
Campanha-Versiani, L., Pereira, D. A. G., Ribeiro-Samora, G. A., Ramos, A. V., Diniz, M. F. H. D. S., Marco, L. A. D., & Soares, M. M. S. (2017) · Obesity Surgery · doi:10.1007/s11695-017-2618-5 · Cited by 93 · see citing works
The Impact of Fat and Obesity on Bone Microarchitecture and Strength in Children
Farr, J. N., & Dimitri, P. (2016) · Calcified Tissue International · doi:10.1007/s00223-016-0218-3 · Cited by 88 · see citing works
“Moreover, bone loss at both peripheral and central skeletal locations persists beyond the period of weight loss implying that additional mechanisms may be responsible for bone loss following bariatric surgery that include nutritional deficiencies, and alterations in adipokines and gut-derived appetite-regulatory hormo…”
BackgroundCardiovascular effects of bariatric surgery
Beamish, A. J., Olbers, T., Kelly, A. S., & Inge, T. H. (2016) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2016.162 · Cited by 84 · see citing works
Murai, I. H., Roschel, H., Dantas, W. S., Gil, S. D. S., Merege-Filho, C. A. A., de Cleva, R., de Sá‐Pinto, A. L., Lima, F., Santo, M. A., Benatti, F. B., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-00074 · Cited by 84 · see citing works
Vitamin D alteration associated with obesity and bariatric surgery
Lespessailles, É., & Toumi, H. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370216688567 · Cited by 77 · see citing works
“Although consecutive to bariatric surgery nutritional deficiencies are well-documented, the literature emphasizes methodological weaknesses in studies addressing the phosphocalcic metabolism and bone sounding in patients who have had bariatric surgery.(50,51) The limitations of the studies in terms of interpretation o…”
BackgroundDivergent Effects of Obesity on Bone Health
Gower, B. A., & Casazza, K. (2013) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2013.08.010 · Cited by 72 · see citing works
Ahlin, S., Peltonen, M., Sjöholm, K., Anveden, Å., Jacobson, P., Andersson‐Assarsson, J. C., Taube, M., Larsson, I., Lohmander, S. L., Näslund, I., et al. (2020) · Journal of Internal Medicine · doi:10.1111/joim.13020 · Cited by 70 · see citing works
Thin bones: Vitamin D and calcium handling after bariatric surgery
Corbeels, K., Verlinden, L., Lannoo, M., Simoens, C., Matthys, C., Verstuyf, A., Meulemans, A., Carmeliet, G., & der Schueren, B. V. (2018) · Bone Reports · doi:10.1016/j.bonr.2018.02.002 · Cited by 67 · see citing works
“These hormonal changes include reduced sex steroid production (testosterone and oestradiol) (Sainsbury and Zhang, 2012) and alterations in the secretion of gut-derived (Glucagon-like peptide 1 (GLP-1), peptide YY (PYY) and ghrelin) and adipocytic (leptin and adiponectin) hormones (Sainsbury and Zhang, 2012; Brzozowska…”
BackgroundHerman, K. M., Carver, T. E., Christou, N. V., & Andersen, R. E. (2014) · Obesity Surgery · doi:10.1007/s11695-014-1212-3 · Cited by 66 · see citing works
“PA also attenuates the losses of metabolically active lean body tissue and bone mineral density accompanying large weight losses [40, 41].”
BackgroundBone mineral density after bariatric surgery. A systematic review
Rodríguez‐Carmona, Y., López‐Alavez, F. J., Garay, A. G. G., Galicia, C. S., Meléndez, G., & Serralde-Zúñiga, A. E. (2014) · International Journal of Surgery · doi:10.1016/j.ijsu.2014.08.002 · Cited by 65 · see citing works
Vitamin D and intestinal calcium transport after bariatric surgery
Schafer, A. L. (2016) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2016.12.012 · Cited by 62 · see citing works
Nutrition in Pregnancy Following Bariatric Surgery
Slater, C., Morris, L. C., Ellison, J., & Syed, A. A. (2017) · Nutrients · doi:10.3390/nu9121338 · Cited by 56 · see citing works
“A recent review addresses the effects of bariatric surgery on bone health [50].”
BackgroundCalcium metabolism, vitamin D and bone mineral density after bariatric surgery
Costa, T. M. D. R. L., Paganotto, M., Radominski, R. B., Kulak, C. A. M., & Borba, V. C. (2014) · Osteoporosis International · doi:10.1007/s00198-014-2962-4 · Cited by 54 · see citing works
Kim, J. J., Nimeri, A. A., Khorgami, Z., Chaar, M. E., Galvez, A., & Vosburg, R. W. (2020) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2020.09.031 · Cited by 53 · see citing works
“Measurements of bone markers can be utilized to assess bone turnover in RYGB patients, as increased bone turnover has been reported to occur as early as 3 months after surgery and may still be present for years [36].”
BackgroundInfluentialCytokines and Hormones That Contribute to the Positive Association between Fat and Bone
Naot, D., & Cornish, J. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00070 · Cited by 52 · see citing works
“Cell Mol Life Sci (2013) 70(13):2331–49.”
InfluentialFernando Carrasco, N., Basfi-fer, K., Rojas, P., Csendes, A., Papapietro, K., Codoceo, J., Inostroza, J., Krebs, N. F., Westcott, J., Miller, L. V., et al. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy071 · Cited by 48 · see citing works
Yu, E. W.-Y., Kim, S. C., Sturgeon, D. J., Lindeman, K. G., & Weissman, J. S. (2019) · JAMA Surgery · doi:10.1001/jamasurg.2019.1157 · Cited by 48 · see citing works
Grace, P. D. C., Vincent, R. P., & Aylwin, S. J. B. (2013) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2013.07.017 · Cited by 45 · see citing works
“Vitamin D insufficiency is widespread [1], particularly in Northern Europe, and data from a United Kingdom (U.”
BackgroundResultInfluentialNeuroendocrine adaptations to bariatric surgery
Dixon, J. B., Lambert, É., & Lambert, G. W. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.05.033 · Cited by 45 · see citing works
“…for example lowering of ghrelin, a rise in leptin, and a rise in PYY along with altered calcium absorption following SG may be predicted to increase risk, and historically post gastrectomy patients have a high risk of osteopenia and fractures (Zittel et al., 1997) (Brzozowska et al., 2013).”
Metabolic Effects of Bariatric Surgery
Sinclair, P., Docherty, N. G., & le Roux, C. W. (2017) · Clinical Chemistry · doi:10.1373/clinchem.2017.272336 · Cited by 42 · see citing works
Weight loss outcomes and complications from bariatric surgery in the super super obese
Serrano, O. K., Tannebaum, J. E., Cumella, L., Choi, J., Vemulapalli, P., Melvin, W. S., & Camacho, D. R. (2015) · Surgical Endoscopy · doi:10.1007/s00464-015-4509-y · Cited by 39 · see citing works
“their sequelae [4–10].”
Jørgensen, A. P., Ueland, T., Sode-Carlsen, R., Schreiner, T., Rabben, K. F., Farholt, S., Höybye, C., Christiansen, J. S., & Bollerslev, J. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3378 · Cited by 36 · see citing works
The associations of gut microbiota, endocrine system and bone metabolism
Tu, Y., Kuang, X., Zhang, L., & Xu, X. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1124945 · Cited by 34 · see citing works
Guerrero‐Pérez, F., Casajoana, A., Gómez‐Vaquero, C., Virgili, N. M., López‐Urdiales, R., Hernández-Montoliu, L., Pujol-Gebellí, J., Osorio, J., Alves, C., Pérez-Maraver, M., et al. (2019) · Obesity Surgery · doi:10.1007/s11695-019-04127-5 · Cited by 34 · see citing works
Roux-en-Y gastric bypass and gastric sleeve surgery result in long term bone loss
Brzozowska, M. M., Tran, T. S., Bliuc, D., Jorgensen, J. O., Talbot, M. L., Fenton‐Lee, D., Chen, W., Hong, A., Viardot, A., White, C., et al. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-00660-x · Cited by 35 · see citing works
Self-citationDilemmas in the Management of Osteoporosis in Younger Adults
Herath, M., Cohen, A., Ebeling, P. R., & Milat, F. (2021) · JBMR Plus · doi:10.1002/jbm4.10594 · Cited by 33 · see citing works
“Because the bone loss persists at 6 months despite weight stabilization, it is hypothesized that hormonal influences contribute to ongoing deterioration in bone.((98)) Solid organ and bone marrow stem cell transplantation Studies which exclusively investigate YAs are limited in this population.”
BackgroundXie, W., Han, Y., Li, F., Gu, X., Su, D., Yu, W., Li, Z., & Xiao, J. (2019) · Calcified Tissue International · doi:10.1007/s00223-019-00647-5 · Cited by 32 · see citing works
The Skeletal Consequences of Bariatric Surgery
Krez, A. N., & Stein, E. M. (2020) · Current Osteoporosis Reports · doi:10.1007/s11914-020-00579-2 · Cited by 32 · see citing works
Wu, K. C., Cao, S., Weaver, C. M., King, N. J., Patel, S., Kim, T. Y., Black, D. M., Kingman, H., Shafer, M. M., Rogers, S. J., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac579 · Cited by 29 · see citing works
Cadart, O., Degrandi, O., Barnetche, T., Mehsen-Cêtre, N., Monsaingeon, M., Pupier, É., Bosc, L., Collet, D., Gronnier, C., Trémollières, F., et al. (2020) · Obesity Surgery · doi:10.1007/s11695-020-04568-3 · Cited by 26 · see citing works
“The negative skeletal effects of bariatric surgery are presumably multifactorial and are not yet fully understood [19, 33, 35, 36].”
BackgroundHarper, C., Pattinson, A. L., Fernando, H. A., Zibellini, J., Seimon, R. V., & Sainsbury, A. (2016) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2016-0025 · Cited by 26 · see citing works
“In addition, stratification by GLP-1 receptor agonist type used (liraglutide or exenatide), revealed no decrease or increase in the risk of fracture [87].”
BackgroundInfluentialSelf-citationBone Density and Trabecular Morphology at Least 10 Years After Gastric Bypass and Gastric Banding
Lindeman, K. G., Rushin, C. C., Cheney, M. C., Bouxsein, M., Hutter, M. M., & Yu, E. W.-Y. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4112 · Cited by 26 · see citing works
“In addition, it is unknown whether the accelerated bone loss observed after bariatric surgery is due to physiologicallyappropriate adaptations to surgery-induced weight loss, or whether it represents a pathologic condition.((2,3,19)) Mechanical unloading of the skeleton occurs during all forms of weight loss,((20)) an…”
BackgroundUncoupling protein-1 is protective of bone mass under mild cold stress conditions
Nguyen, A., Lee, N. J., Wee, N. K. Y., Zhang, L., Enriquez, R. F., Khor, E. C., Nie, T., Wu, D., Sainsbury, A., Baldock, P. A. J., et al. (2015) · Bone · doi:10.1016/j.bone.2015.05.037 · Cited by 25 · see citing works
“In recent years it has become increasingly apparent that the interaction between skeletal and energy homeostasis is vastly more complex than was appreciated, with both systems releasing factors that can concurrently affect either system [44].”
BackgroundSelf-citationBone Health after Bariatric Surgery
Shahraki, M. S., Mahmoudieh, M., Kalidari, B., Melali, H., Mousavi, M., Abadi, M. R. G., Mirhosseini, S. H., & Dehabadi, S. A. M. (2022) · Advanced Biomedical Research · doi:10.4103/abr.abr_182_21 · Cited by 24 · see citing works
“Visfatin and Resistin indicate different effects on BMD and are generally expected to inhibit bone mass.[11] Furthermore, in the”
BackgroundInfluentialKim, M. S., Kim, J. Y., Song, Y. S., Hong, S., Won, H., Kim, W. J., Kwon, Y., Ha, J., Fiedorowicz, J. G., Solmi, M., et al. (2023) · Obesity Reviews · doi:10.1111/obr.13670 · Cited by 23 · see citing works
Micronutrient Deficiencies Following Minimally Invasive Esophagectomy for Cancer
Janssen, H. J. B., Fransen, L. F. C., Ponten, J. E. H., Nieuwenhuijzen, G. A. P., & Luyer, M. D. P. (2020) · Nutrients · doi:10.3390/nu12030778 · Cited by 20 · see citing works
“Nonetheless, similar to other types of gastric surgery [17,21], Elliot et al.”
ResultApproaches to obesity management
Sweeting, A., & Caterson, I. D. (2017) · Internal Medicine Journal · doi:10.1111/imj.13474 · Cited by 20 · see citing works
Bone mineral density changes after bariatric surgery
Ieong, K., Ardila-Gatas, J., Yang, J., Zhang, X., Tsui, S. T., Spaniolas, K., & Pryor, A. D. (2020) · Surgical Endoscopy · doi:10.1007/s00464-020-07953-2 · Cited by 20 · see citing works
Exercise Is Key to Sustaining Metabolic Gains After Bariatric Surgery
Gualano, B., Kirwan, J. P., & Roschel, H. (2021) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000253 · Cited by 19 · see citing works
Body Weight/Composition and Weight Change: Effects on Bone Health
Shapses, S. A., & Cifuentes, M. (2014) · Springer eBooks · doi:10.1007/978-1-4939-2001-3_33 · Cited by 19 · see citing works
Bariatric Surgery: Targeting pancreatic β cells to treat type II diabetes
Liu, T., Zou, X., Ruze, R., & Xu, Q. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1031610 · Cited by 22 · see citing works
“Long-term complications include gallstone disease (25) and bone loss (26).”
BackgroundPaccou, J., Thuillier, D., Courtalin, M., Pigny, P., Labreuche, J., Cortet, B., & Pattou, F. N. (2021) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2021.12.004 · Cited by 18 · see citing works
Bariatric Surgery: Bad to the Bone, Part 2.
Pizzorno, L. (2016) · PubMed Central · Cited by 17 · see citing works
Influence of Hormonal Appetite and Energy Regulators on Bone
Khor, E. C., Wee, N. K. Y., & Baldock, P. A. J. (2013) · Current Osteoporosis Reports · doi:10.1007/s11914-013-0157-0 · Cited by 17 · see citing works
Self-citationOsteoporosis: From Bone Biology to Individual Treatment Decision
Gonçalves, M. J., Rodrigues, A. M., Canhão, H. M., & Fonseca, J. E. (2013) · Acta Médica Portuguesa · doi:10.20344/amp.4271 · Cited by 15 · see citing works
Lin, S., Yang, N., Guan, W., & Liang, H. (2019) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2019.03.027 · Cited by 16 · see citing works
Svanevik, M., Risstad, H., Hofsø, D., Blom-Høgestøl, I. K., Kristinsson, J. A., Sandbu, R., Småstuen, M. C., Thorsby, P. M., Mala, T., & Hjelmesaeth, J. S. (2019) · Obesity Surgery · doi:10.1007/s11695-019-03909-1 · Cited by 16 · see citing works
Guerrero‐Pérez, F., Casajoana, A., Gómez‐Vaquero, C., Virgili, N. M., López‐Urdiales, R., Hernández-Montoliu, L., Pujol-Gebellí, J., Osorio, J., Prats, A. R., Vidal‐Alabró, A., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9061830 · Cited by 16 · see citing works
“Bariatric surgery produces detrimental effects on bone health and there is a significant and non-uniform reduction in BMD across different bone sites [3,16,41,42].”
BackgroundWei, J., Hunter, D. J., Lane, N. E., Wu, J., Zeng, C., Lei, G., & Zhang, Y. (2023) · Arthritis & Rheumatology · doi:10.1002/art.42754 · Cited by 15 · see citing works
“42 Taken together, the discordant fi ndings between the all-cause mortality outcome and each of the other outcomes in the fast rate of weight loss group compared with the reference group might be attributed to the potential drawbacks (eg, myo fi brilla damage and increased risk of metabolic bone…”
BackgroundLong-Term Bone Health After Roux-en-Y Gastric Bypass: A Pilot Study
Cook, F., Khanna, I., Giordano, J., Matarese, L. E., & Hudson, S. (2017) · Endocrine Practice · doi:10.4158/ep171823.or · Cited by 15 · see citing works
Physical activity and sitting time in bariatric surgery patients 1–16 years post‐surgery
Herman, K. M., Carver, T. E., Christou, N. V., & Andersen, R. E. (2014) · Clinical Obesity · doi:10.1111/cob.12069 · Cited by 13 · see citing works
“PA increases total daily energy expenditure, improves abdominal visceral fat loss (23) and attenuates the loss of lean muscle mass and bone mineral density which accompanies large weight losses (24,25), thus helping to optimize energy balance and physical functioning compared with weight loss without exercise.”
BackgroundEffects of bariatric surgery on bone
Uebelhart, B. (2016) · Joint Bone Spine · doi:10.1016/j.jbspin.2016.02.013 · Cited by 13 · see citing works
The impact of obesity on bone health: an overview
Mendonça, F. M., Soares, R. A., Carvalho, D. M., & Freitas, P. (2022) · Endokrynologia Polska · doi:10.5603/ep.a2022.0063 · Cited by 13 · see citing works
Bariatric Surgery: Bad to the Bone, Part 1.
Pizzorno, L. (2016) · Europe PMC (PubMed Central) · Cited by 12 · see citing works
Bsm1 Vitamin D Receptor Polymorphism and Calcium Homeostasis Following Bariatric Surgery
Alexandrou, A. P., Armeni, E., Kaparos, G., Rizos, D., Tsoka, E., Deligeoroglou, E., Creatsa, M. G., Augoulea, A., Diamantis, T., & Lambrinoudaki, I. V. (2014) · Journal of Investigative Surgery · doi:10.3109/08941939.2014.943857 · Cited by 12 · see citing works
“significant associations between post-surgical weight loss and increased markers of bone remodeling [3, 39, 40], which is in agreement with our findings.”
BackgroundResultInfluentialLima, T. P., Nicoletti, C. F., Marchini, J. S., Salgado, W., & Nonino, C. B. (2014) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2014.08.002 · Cited by 11 · see citing works
Outcomes of laparoscopic sleeve gastrectomy in elderly obese Japanese patients
Hayashi, A., Maeda, Y., Takemoto, M., Tokuyama, H., Koide, H., Kitahara, A., Hayashi, H., Kitamoto, T., Yamaga, M., Kobayashi, K., et al. (2017) · Geriatrics and gerontology international/Geriatrics & gerontology international · doi:10.1111/ggi.13022 · Cited by 11 · see citing works
Zarshenas, N., Tapsell, L. C., Batterham, M. J., Neale, E. P., & Talbot, M. L. (2022) · Nutrition & Dietetics · doi:10.1111/1747-0080.12747 · Cited by 10 · see citing works
“suggests a strong inverse relationship between total fat mass and bone mineral density, discussing the consequence of obesity and its related metabolic syndrome in bone formation rate, bone mineral density and increasing fractures.(30) Given the impact of weight loss on metabolic bone health following bariatric surger…”
BackgroundBariatric surgery, weight loss and bone
White, C. P. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.189 · Cited by 10 · see citing works
VITAMIN D DEFICIENCY AND PARATOHOMMONIUM INCREASE IN LATE POSTOPERATIVE GASTRIC BYPASS IN ROUX-EN-Y
Mônaco-Ferreira, D. V., Leandro‐Merhi, V. A., Aranha, N. C., Brandalise, A., & Brandalise, N. A. (2018) · ABCD Arquivos Brasileiros de Cirurgia Digestiva (São Paulo) · doi:10.1590/0102-672020180001e1407 · Cited by 10 · see citing works
“2/5 ABCD Arq Bras Cir Dig 2018;31(4):e1407”
InfluentialRobinson, D. E., Douglas, I., Tan, G. D., Delmestri, A., Judge, A., Cooper, C. C., Javaid, M. K., Strauss, V. Y., & Prieto‐Alhambra, D. (2021) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4405 · Cited by 9 · see citing works
“The mechanisms behind the identified increased incidence and potential predictors of major fractures are not known.((23)) After bariatric surgery, patients experience nutritional deficits, including deficits in the absorption of calcium and vitamin D, key nutrients for bone health.”
BackgroundHany, M., Wuyts, S. C. M., Abouelnasr, A. A., Zidan, A., Demerdash, H. M., Hussein, H. A. S. M., Arida, R. E., Elsharkawi, S. M., Kramers, C., & Torensma, B. (2024) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2024.10.034 · Cited by 8 · see citing works
Hammoud, E., Jacob, C., Pinti, A., Khalil, N., Hage, Z. E., Toumi, H., & Hage, R. E. (2024) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2024.101556 · Cited by 8 · see citing works
The Impact of Bariatric Surgery on Bone Health: State of the Art and New Recognized Links
Mendonça, F. M., Soares, R. A., Carvalho, D. M., & Freitas, P. (2022) · Hormone and Metabolic Research · doi:10.1055/a-1767-5581 · Cited by 8 · see citing works
“This hormone – which is produced in the gastric antrum and fundus – is thought to be an important player in the long-term maintenance of energy stores as it stimulates appetite and decreases energy expenditure [106].”
BackgroundHofsø, D., Bollerslev, J., Sandbu, R., Jørgensen, A. P., Godang, K., Hjelmesaeth, J. S., & Ueland, T. (2016) · Endocrine · doi:10.1007/s12020-016-0903-z · Cited by 8 · see citing works
The hunger games of skeletal metabolism
Wee, N. K. Y., & Baldock, P. A. J. (2014) · BoneKEy Reports · doi:10.1038/bonekey.2014.83 · Cited by 7 · see citing works
“These responses have great interest in terms of obesity and glycaemic control; however, they are also likely to shed light upon their influence upon bone mass (reviewed in Brzozowska et al.(70)).”
BackgroundSelf-citationSchakarowski, F. B., Padoin, A. V., Mottin, C. C., & de Castro, E. K. (2018) · Temas em Psicologia · doi:10.9788/tp2018.1-13pt · Cited by 6 · see citing works
Transient osteoporosis of the hip after bariatric surgery
Hong, C. S., Bergen, M. A., & Watters, T. S. (2018) · Arthroplasty Today · doi:10.1016/j.artd.2018.10.010 · Cited by 5 · see citing works
“data on the direct effects of bariatric surgery on bone density in patients postoperatively [24], so it is unclear if this could be a factor contributing to TOH in this patient population.”
Background18. Diet-induced obesity alters skeletal microarchitecture and the endocrine activity of bone
Wee, N. K. Y., Herzog, H., & Baldock, P. A. J. (2016) · Wageningen Academic Publishers eBooks · doi:10.3920/978-90-8686-823-0_18 · Cited by 4 · see citing works
Self-citationThe incidence of fractures following bariatric surgery: A systematic review
Marcil, G., Bourget-Murray, J., Shinde, S., Switzer, N. J., Debru, E., Church, N. G., Mitchell, P., Reso, A., & Gill, R. S. (2018) · International Journal of Surgery Open · doi:10.1016/j.ijso.2018.08.005 · Cited by 4 · see citing works
de Almeida, C. M., Lopes, K. G., Bezerra, M. D. C. T., Leal, P. R. F., Bouskela, E., da Gama, E. M. F., Farias, M. L. F., Madeira, M., & Kraemer‐Aguiar, L. G. (2026) · Obesity · doi:10.1002/oby.70132 · Cited by 3 · see citing works
Effects of bariatric surgery on bone metabolism: focusing on vitamin D
Avdeeva, V. A., Suplotova, L. A., & Rozhinskaya, L. Y. (2022) · Obesity and metabolism · doi:10.14341/omet12702 · Cited by 6 · see citing works
Fernando, H. A., Zibellini, J., Hsu, M. S. H., Seimon, R. V., Nguyen, A., & Sainsbury, A. (2015) · Expert Review of Endocrinology & Metabolism · doi:10.1586/17446651.2015.1001741 · Cited by 3 · see citing works
“bariatric surgery is increasingly being linked to bone loss [5,6], and some but not all studies suggest that even a milder form of obesity treatment, diet-induced weight loss, reduces BMD [7,17], particularly when physical activity is not an integral part of the program [7,18].”
BackgroundSelf-citationCirurgia bariátrica no tratamento da obesidade: impacto sobre o metabolismo ósseo
Sarmento, R. A., Casagrande, D. S., & Schaan, B. D. (2014) · Revista Hospital Universitário Pedro Ernesto · doi:10.12957/rhupe.2014.9811 · Cited by 3 · see citing works
Linden, B. C., & Barnett, S. J. (2015) · Springer eBooks · doi:10.1007/978-3-319-04343-2_77 · Cited by 3 · see citing works
Obesity and Fractures: Between Black and White Aspects
Carşote, M., & Pereţianu, D. (2015) · Journal of Obesity & Weight loss Therapy · doi:10.4172/2165-7904.1000288 · Cited by 2 · see citing works
“Also the neurohormonal status is changed as well as bone turnover markers levels [76-78].”
BackgroundStapleton, J. R., Ard, J. D., Beavers, D. P., Cogdill, L. S., Fernandez, A., Howard, M. J., Justice, J. N., Lynch, S. D., Newman, J. J., Weaver, A. A., et al. (2023) · Contemporary Clinical Trials Communications · doi:10.1016/j.conctc.2023.101181 · Cited by 2 · see citing works
Metabolic Surgery for Dabetes Mellitus between Benefits and Risks
Fica, S. V. (2015) · Acta Endocrinologica (Bucharest) · doi:10.4183/aeb.2015.212 · Cited by 2 · see citing works
“The consequence of these is a substantial rise in parathyroid hormone concentrations, documented by many studies (52), which has deleterious consequences especially on cortical bone.”
Background
- Authors
- Brzozowska, M. M., Sainsbury, A., Eisman, J. A., Baldock, P. A., & Center, J. R.
- Affiliations
- Garvan Institute of Medical Research (AU)
- The University of Sydney (AU)
- Osteoporosis and Bone Biology Division Garvan Institute of Medical Research Sydney Australia
- Venue
- Obesity Reviews
- Publisher
- Wiley
- Published
- 2012-10-25
- Volume
- 14
- Issue
- 1
- Pages
- 52-67
- ISSN
- 1467-7881 (ISSN-L)
- 1467-789X
- OpenAlex
- W1909242889
- Cited by
- 128
- References
- 206
- Citations by year
- 2026: 3 · 2024: 3 · 2023: 6 · 2022: 9 · 2021: 6 · 2020: 12 · 2019: 9 · 2018: 10 · 2017: 11 · 2016: 14 · 2015: 13 · 2014: 20 · 2013: 12
- FWCI
- 2.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Obesity Reviews (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion)
- The Sydney eScholarship Repository (The University of Sydney) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Bariatric Surgery and Outcomes
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Keywords
- bariatric surgery, bone loss, obesity, bone metabolism, nutritional deficiency, rapid weight loss, adipokines, gastrointestinal hormones, appetite regulation, energy homeostasis, bone homeostasis, abdominal obesity, bone marrow fat, osteoporosis, fracture risk
- MeSH terms
- Avitaminosis, Bone and Bones, Bone Resorption, Gastrointestinal Hormones, Humans, Nutritional Requirements, Nutritional Status, Obesity, Morbid, Osteoporosis, Weight Loss, Bariatric Surgery
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