The Impact of Interventional Weight Loss on Bone Marrow Adipose Tissue in People Living with Obesity and Its Connection to Bone Metabolism
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
37960254
PubMed Central
PMC10650495
DOI
10.3390/nu15214601
PII: nu15214601
Knihovny.cz E-zdroje
- Klíčová slova
- bone marrow adipose tissue, bone mineral density, clinical trials, fractures, imaging, metabolic and bariatric surgery, obesity, osteoporosis, weight loss,
- MeSH
- hmotnostní úbytek MeSH
- kostní denzita MeSH
- kostní dřeň * metabolismus MeSH
- lidé MeSH
- obezita metabolismus MeSH
- tuková tkáň * MeSH
- Check Tag
- lidé MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
This review focuses on providing physicians with insights into the complex relationship between bone marrow adipose tissue (BMAT) and bone health, in the context of weight loss through caloric restriction or metabolic and bariatric surgery (MBS), in people living with obesity (PwO). We summarize the complex relationship between BMAT and bone health, provide an overview of noninvasive imaging techniques to quantify human BMAT, and discuss clinical studies measuring BMAT in PwO before and after weight loss. The relationship between BMAT and bone is subject to variations based on factors such as age, sex, menopausal status, skeletal sites, nutritional status, and metabolic conditions. The Bone Marrow Adiposity Society (BMAS) recommends standardizing imaging protocols to increase comparability across studies and sites, they have identified both water-fat imaging (WFI) and spectroscopy (1H-MRS) as accepted standards for in vivo quantification of BMAT. Clinical studies measuring BMAT in PwO are limited and have shown contradictory results. However, BMAT tends to be higher in patients with the highest visceral adiposity, and inverse associations between BMAT and bone mineral density (BMD) have been consistently found in PwO. Furthermore, BMAT levels tend to decrease after caloric restriction-induced weight loss. Although weight loss was associated with overall fat loss, a reduction in BMAT did not always follow the changes in fat volume in other tissues. The effects of MBS on BMAT are not consistent among the studies, which is at least partly related to the differences in the study population, skeletal site, and duration of the follow-up. Overall, gastric bypass appears to decrease BMAT, particularly in patients with diabetes and postmenopausal women, whereas sleeve gastrectomy appears to increase BMAT. More research is necessary to evaluate changes in BMAT and its connection to bone metabolism, either in PwO or in cases of weight loss through caloric restriction or MBS, to better understand the role of BMAT in this context and determine the local or systemic factors involved.
Department of Endocrinology Amsterdam UMC University of Amsterdam 1105 AZ Amsterdam The Netherlands
Department of Molecular Medicine Sapienza University of Rome 00161 Rome Italy
Department of Rheumatology MABLab ULR 4490 CHU Lille University Lille 59000 Lille France
Zobrazit více v PubMed
Gadde K.M., Martin C.K., Berthoud H.R., Heymsfield S.B. Obesity: Pathophysiology and Management. J. Am. Coll. Cardiol. 2018;71:69–84. doi: 10.1016/j.jacc.2017.11.011. PubMed DOI PMC
Pasquali R., Casanueva F., Haluzik M., van Hulsteijn L., Ledoux S., Monteiro M.P., Salvador J., Santini F., Toplak H., Dekkers O.M. European Society of Endocrinology Clinical Practice Guideline: Endocrine work-up in obesity. Eur. J. Endocrinol. 2020;182:G1–G32. doi: 10.1530/EJE-19-0893. PubMed DOI
Chang S.H., Stoll C.R., Song J., Varela J.E., Eagon C.J., Colditz G.A. The effectiveness and risks of bariatric surgery: An updated systematic review and meta-analysis, 2003–2012. JAMA Surg. 2014;149:275–287. doi: 10.1001/jamasurg.2013.3654. PubMed DOI PMC
Sjöström L., Peltonen M., Jacobson P., Ahlin S., Andersson-Assarsson J., Anveden Å., Bouchard C., Carlsson B., Karason K., Lönroth H., et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascu-lar and macrovascular complications. JAMA. 2014;311:2297–2304. doi: 10.1001/jama.2014.5988. PubMed DOI
Kadowaki T., Isendahl J.K., Khalid U., Lee S.W., Nishida T., Ogawa W., Tobe K., Yamauchi T., Lim S. Semaglutide once a week in adults with overweight or obesity, with or without type 2 diabetes in an east Asian population (STEP 6): A randomised, double-blind, double-dummy, placebo-controlled, phase 3a trial. Lancet Diabetes Endocrinol. 2022;10:193–206. doi: 10.1016/S2213-8587(22)00008-0. PubMed DOI
Rubino D.M., Grenway F.L., Khalid O., O’Neil P.M., Rosenstock J., Sørrig R., Wadden T.A., Wizert A., Garvey W.T., STEP 8 Investigators Effect of weekly subcutaneous Semaglutide vs daily Liraglutide on body weight in adults with overweight or obesity without diabetes. The Step 8 Randomized Clinical Study. JAMA. 2022;327:138–150. doi: 10.1001/jama.2021.23619. PubMed DOI PMC
Lespessailles E., Paccou J., Javier R.M., Thomas T., Cortet B., GRIO Scientific Committee GRIO Scientific Committee. Obesity, Bariatric Surgery, and Fractures. J. Clin. Endocrinol. Metab. 2019;104:4756–4768. doi: 10.1210/jc.2018-02084. PubMed DOI
Paccou J., Caiazzo R., Lespessailles E., Cortet B. Bariatric Surgery and Osteoporosis. Calcif. Tissue Int. 2022;110:576–591. doi: 10.1007/s00223-020-00798-w. PubMed DOI
Papageorgiou M., Kerschan-Schindl K., Sathyapalan T., Pietschmann P. Is Weight Loss Harmful for Skeletal Health in Obese Older Adults? Gerontology. 2020;66:2–14. doi: 10.1159/000500779. PubMed DOI
Shanbhogue V.V., Støving R.K., Frederiksen K.H., Hanson S., Brixen K., Gram J., Jørgensen N.R., Hansen S. Bone structural changes after gastric bypass surgery evaluated by HR-pQCT: A two-year longitudinal study. Eur. J. Endocrinol. 2017;176:685–693. doi: 10.1530/EJE-17-0014. PubMed DOI PMC
Paccou J., Martignène N., Lespessailles E., Babykina E., Pattou F., Cortet B., Ficheur G. Gastric bypass but not sleeve gastrectomy increases risk of major osteoporotic fracture: French population-based cohort study. J. Bone Miner Res. 2020;35:1415–1423. doi: 10.1002/jbmr.4012. PubMed DOI
Khalid S.I., Omotosho P.A., Spagnoli A., Torquati A. Association of Bariatric Surgery with Risk of Fracture in Patients with Severe Obesity. JAMA Netw. Open. 2020;3:e207419. doi: 10.1001/jamanetworkopen.2020.7419. PubMed DOI PMC
Paccou J., Tsourdi E., Meier C., Palermo A., Pepe J., Body J.-J., Zillikens M.C. Bariatric surgery and skeletal health: A narrative review and position statement for management by the European Calcified Tissue Society (ECTS) Bone. 2021;154:116236. doi: 10.1016/j.bone.2021.116236. PubMed DOI
Villareal D.T., Shah K., Banks M.R., Sinacore D.R., Klein S. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: A one-year randomized controlled trial. J. Clin. Endocrinol. Metab. 2008;93:2181–2187. doi: 10.1210/jc.2007-1473. PubMed DOI PMC
Paccou J., Penel G., Chauveau C., Cortet B., Hardouin P. Marrow adiposity and bone: Review of clinical implications. Bone. 2019;118:8–15. doi: 10.1016/j.bone.2018.02.008. PubMed DOI
Veldhuis-Vlug A.G., Rosen C.J. Clinical implications of bone marrow adiposity. J. Intern. Med. 2018;283:121–139. doi: 10.1111/joim.12718. PubMed DOI PMC
Beekman K.M., Duque G., Corsi A., Tencerova M., Bisschop P.H., Paccou J. Osteoporosis and Bone Marrow Adipose Tissue. Curr. Osteoporos. Rep. 2023;21:45–55. doi: 10.1007/s11914-022-00768-1. PubMed DOI
Li Z., Rosen C.J. The Multifaceted Roles of Bone Marrow Adipocytes in Bone and Hematopoietic Homeostasis. J. Clin. Endocrinol. Metab. 2023:dgad355. doi: 10.1210/clinem/dgad355. PubMed DOI
Paccou J., Hardouin P., Cotten A., Penel G., Cortet B. The Role of Bone Marrow Fat in Skeletal Health: Usefulness and Perspectives for Clinicians. J. Clin. Endocrinol. Metab. 2015;100:3613–3621. doi: 10.1210/jc.2015-2338. PubMed DOI
Cawthorn W.P., Scheller E.L., Learman B.S., Parlee S.D., Simon B.R., Mori H., Ning X., Bree A.J., Schell B., Broome D.T., et al. Bone Marrow Adipose Tissue Is an Endocrine Organ that Contributes to Increased Circulating Adiponectin during Caloric Restriction. Cell Metab. 2014;20:368–375. doi: 10.1016/j.cmet.2014.06.003. PubMed DOI PMC
Paccou J., Badr S., Lombardo D., Khizindar H., Deken V., Ruschke S., Karampinos D.C., Cotten A., Cortet B. Bone Marrow Adiposity and Fragility Fractures in Postmenopausal Women: The ADIMOS Case-Control Study. J. Clin. Endocrinol. Metab. 2023;108:2526–2536. doi: 10.1210/clinem/dgad195. PubMed DOI
Schwartz A.V. Marrow fat and bone: Review of clinical findings. Front. Endocrinol. 2015;6:40. doi: 10.3389/fendo.2015.00040. PubMed DOI PMC
Woods G.N., Ewing S.K., Schafer A.L., Gudnason V., Sigurdsson S., Lang T., Hue T.F., Kado D.M., Vittinghoff E., Rosen C., et al. Saturated and Unsaturated Bone Marrow Lipids Have Distinct Effects on Bone Density and Fracture Risk in Older Adults. J. Bone Miner. Res. 2022;37:700–710. doi: 10.1002/jbmr.4504. PubMed DOI PMC
Li Z., Bowers E., Zhu J., Yu H., Hardij J., Bagchi D.P., Mori H., Lewis K.T., Granger K., Schill R.L., et al. Lipolysis of bone marrow adipocytes is required to fuel bone and the marrow niche during energy deficits. eLife. 2022;11:e78496. doi: 10.7554/eLife.78496. PubMed DOI PMC
Fazeli P.K., Bredella M.A., Pachon-Peña G., Zhao W., Zhang X., Faje A.T., Resulaj M., Polineni S.P., Holmes T.M., Lee H., et al. The dynamics of human bone marrow adipose tissue in response to feeding and fasting. J. Clin. Investig. 2021;6:138636. doi: 10.1172/jci.insight.138636. PubMed DOI PMC
Craft C.S., Li Z., MacDougald O.A., Scheller E.L. Molecular differences between subtypes of bone marrow adipocytes. Curr. Mol. Biol. Rep. 2018;4:16–23. doi: 10.1007/s40610-018-0087-9. PubMed DOI PMC
Sollmann N., Löffler M.T., Kronthaler S., Böhm C., Dieckmeyer M., Ruschke S., Kirschke J.S., Carballido-Gamio J., Karampinos D.C., Krug R., et al. MRI-Based Quantitative Osteoporosis Imaging at the Spine and Femur. J. Magn. Reson. Imaging. 2021;54:12–35. doi: 10.1002/jmri.27260. PubMed DOI
Beekman K.M., Regenboog M., Nederveen A.J., Bravenboer N., Heijer M.D., Bisschop P.H., Hollak C.E., Akkerman E.M., Maas M. Gender- and Age-Associated Differences in Bone Marrow Adipose Tissue and Bone Marrow Fat Unsaturation Throughout the Skeleton, Quantified Using Chemical Shift Encoding-Based Water–Fat MRI. Front. Endocrinol. 2022;13:815835. doi: 10.3389/fendo.2022.815835. PubMed DOI PMC
Tratwal J., Labella R., Bravenboer N., Kerckhofs G., Douni E., Scheller E.L., Badr S., Karampinos D.C., Beck-Cormier S., Palmisano B., et al. Reporting Guidelines, Review of Methodological Standards, and Challenges Toward Harmonization in Bone Marrow Adiposity Research. Report of the Methodologies Working Group of the International Bone Marrow Adiposity Society. Front. Endocrinol. 2020;11:65. doi: 10.3389/fendo.2020.00065. PubMed DOI PMC
Lecka-Czernik B., Stechschulte L.A., Czernik P.J., Dowling A.R. High bone mass in adult mice with diet-induced obesity results from a combination of initial increase in bone mass followed by attenuation in bone formation; implications for high bone mass and decreased bone quality in obesity. Mol. Cell Endocrinol. 2015;410:35–41. doi: 10.1016/j.mce.2015.01.001. PubMed DOI
Doucette C.R., Horowitz M.C., Berry R., MacDougald O.A., Anunciado-Koza R., Koza R.A., Rosen C.J. A High Fat Diet Increases Bone Marrow Adipose Tissue (MAT) But Does Not Alter Trabecular or Cortical Bone Mass in C57BL/6J Mice. J. Cell Physiol. 2015;230:2032–2037. doi: 10.1002/jcp.24954. PubMed DOI PMC
Scheller E.L., Khoury B., Moller K.L., Wee N.K.Y., Khandaker S., Kozloff K.M., Abrishami S.H., Zamarron B.F., Singer K. Changes in Skeletal Integrity and Marrow Adiposity during High-Fat Diet and after Weight Loss. Front. Endocrinol. 2016;7:102. doi: 10.3389/fendo.2016.00102. PubMed DOI PMC
Devlin M.J., Robbins A., Cosman M.N., Moursi C.A., Cloutier A.M., Louis L., Van Vliet M., Conlon C., Bouxsein M.L. Differential effects of high fat diet and diet-induced obesity on skeletal acquisition in female C57BL/6J vs. FVB/NJ Mice. Bone Rep. 2018;8:204–214. doi: 10.1016/j.bonr.2018.04.003. PubMed DOI PMC
Charles A., Mugisha A., Iconaru L., Baleanu F., Benoit F., Surquin M., Bergmann P., Body J.J. Distribution of Fracture Sites in Postmenopausal Overweight and Obese Women: The FRISBEE Study. Calcif. Tissue Int. 2022;111:29–34. doi: 10.1007/s00223-022-00968-y. PubMed DOI
Piotrowska K., Tarnowski M. Bone Marrow Adipocytes—Role in Physiology and Various Nutritional Conditions in Human and Animal Models. Nutrients. 2021;13:1412. doi: 10.3390/nu13051412. PubMed DOI PMC
Li Z., MacDougald O.A. Preclinical models for investigating how bone marrow adipocytes influence bone and hematopoietic cellularity. Best Pract. Res. Clin. Endocrinol. Metab. 2021;35:101547. doi: 10.1016/j.beem.2021.101547. PubMed DOI PMC
Gkastaris K., Goulis D.G., Potoupnis M., Anastasilakis A.D., Kapetanos G. Obesity, osteoporosis and bone metabolism. J. Musculoskelet. Neuronal. Interact. 2020;20:372–381. PubMed PMC
Compston J.E., Watts N.B., Chapurlat R., Cooper C., Boonen S., Greenspan S., Pfeilschifter J., Silverman S., Díez-Pérez A., Lindsay R., et al. Obesity is not protective against fracture in postmenopausal women: GLOW. Am. J. Med. 2011;124:1043–1050. doi: 10.1016/j.amjmed.2011.06.013. PubMed DOI PMC
Johansson H., Kanis J.A., Odén A., McCloskey E., Chapurlat R.D., Christiansen C., Cummings S.R., Diez-Perez A., Eisman J.A., Fujiwara S., et al. A meta-analysis of the association of fracture risk and body mass index in women. J. Bone Miner. Res. 2014;29:223–233. doi: 10.1002/jbmr.2017. PubMed DOI
Cohen A., Dempster D.W., Recker R.R., Lappe J.M., Zhou H., Zwahlen A., Müller R., Zhao B., Lang T., Saeed I., et al. Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: A transiliac bone biopsy study. J. Clin. Endocrinol. Metab. 2013;98:2562–2572. doi: 10.1210/jc.2013-1047. PubMed DOI PMC
Bredella M.A., Torriani M., Ghomi R.H., Thomas B.J., Brick D.J., Gerweck A.V., Rosen C.J., Klibanski A., Miller K.K. Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity. 2011;19:49–53. doi: 10.1038/oby.2010.106. PubMed DOI PMC
Bredella M., Gill C., Gerweck A., Landa M.G., Kumar V., Daley S.M., Torriani M., Miller K.K. Ectopic and Serum Lipid Levels Are Positively Associated with Bone Marrow Fat in Obesity. Radiology. 2013;269:534–541. doi: 10.1148/radiol.13130375. PubMed DOI PMC
Singhal V., Bose A., Liang Y., Srivastava G., Goode S., Stanford F.C., Misra M., Bredella M.A. Marrow adipose tissue in adolescent girls with obesity. Bone. 2019;129:115103. doi: 10.1016/j.bone.2019.115103. PubMed DOI PMC
Singhal V., Flores L.P.T., Stanford F.C., Toth A.T., Carmine B., Misra M., Bredella M.A. Differential associations between appendicular and axial marrow adipose tissue with bone microarchitecture in adolescents and young adults with obesity. Bone. 2018;116:203–206. doi: 10.1016/j.bone.2018.08.009. PubMed DOI PMC
CDC: Centers for Disease Control and Prevention Losing Weight; What Is Healthy Weight Loss? [(accessed on 15 May 2023)]; Available online: http://www.cdc.gov/healthyweight/losing_weight/index.html.
NICE: National Institute for Health and Care Excellence CG43 . Obesity: Guidance on the Prevention, Identification, Assessment and Management of Overweight and Obesity in Adults and Children. NICE; London, UK: 2006.
Verheijden M.W., Bakx J.C., Van Weel C., Koelen M.A., Van Staveren W.A. Role of social support in lifestyle-focussed weight management interventions. Euro. J. Clin. Nutr. 2005;59((Suppl. S1)):179–186. doi: 10.1038/sj.ejcn.1602194. PubMed DOI
Cordes C., Dieckmeyer M., Ott B., Shen J., Ruschke S., Settles M., Eichhorn C., Bauer J.S., Kooijman H., Rummeny E.J., et al. MR-detected changes in liver, abdominal, and vertebral bone marrow fat after a four-week calorie restriction in obese women. J. Magn. Reson. Imaging JMRI. 2015;42:272–1280. doi: 10.1002/jmri.24908. PubMed DOI
Vogt L.J., Steveling A., Meffert P.J., Kromrey M.L., Kessler R., Hosten N., Krüger J., Gärtner S., Aghdassi A.A., Mayerle J., et al. Magnetic resonance imaging of changes in abdominal compartments in obese diabetics during a low-calorie weight-loss program. PLoS ONE. 2016;11:e0153595. doi: 10.1371/journal.pone.0153595. PubMed DOI PMC
Spurny M., Jiang Y., Sowah S.A., Schübel R., Nonnenmacher T., Bertheau R., Kirsten R., Johnson T., Hillengass J., Schlett C.L., et al. Changes in Bone Marrow Fat upon Dietary-Induced Weight Loss. Nutrients. 2020;12:1509. doi: 10.3390/nu12051509. PubMed DOI PMC
Ofir N., Mizrakli Y., Greenshpan Y., Gepner Y., Sharabi O., Tsaban G., Zelicha H., Meir A.Y., Ceglarek U., Stumvoll M., et al. Vertebrae but not femur marrow fat transiently decreases in response to body weight loss in an 18-month randomized control trial. Bone. 2023;171:116727. doi: 10.1016/j.bone.2023.116727. PubMed DOI
Kim T.Y., Schwartz A.V., Li X., Xu K., Black D.M., Petrenko D.M., Stewart L., Rogers S.J., Posselt A.M., Carter J.T., et al. Bone Marrow Fat Changes After Gastric Bypass Surgery Are Associated with Loss of Bone Mass. J. Bone Miner. Res. 2017;32:2239–2247. doi: 10.1002/jbmr.3212. PubMed DOI PMC
Kim T.Y., Schwartz A.V., Li X., Xu K., Kazakia G.J., Grunfeld C., Nissenson R.A., Shoback D.M., Schafer A.L. Bone marrow adipose tissue composition and glycemic improvements after gastric bypass surgery. Bone Rep. 2022;17:101596. doi: 10.1016/j.bonr.2022.101596. PubMed DOI PMC
Beekman K.M., Akkerman E.M., Streekstra G.J., Veldhuis-Vlug A.G., Acherman Y., Gerdes V.E., den Heijer M., Maas M., Bravenboer N., Bisschop P.H. The Effect of Roux-en-Y Gastric Bypass on Bone Marrow Adipose Tissue and Bone Mineral Density in Postmenopausal, Nondiabetic Women. Obesity. 2021;29:1120–1127. doi: 10.1002/oby.23171. PubMed DOI PMC
Blom-Høgestøl I.K., Mala T., Kristinsson J.A., Hauge E., Brunborg C., Gulseth H.L., Eriksen E.F. Changes in Bone Marrow Adipose Tissue One Year After Roux-en-Y Gastric Bypass: A Prospective Cohort Study. J. Bone Miner. Res. 2019;34:1815–1823. doi: 10.1002/jbmr.3814. PubMed DOI
Bredella M.A., Singhal V., Hazhir Karzar N., Animashaun A., Bose A., Stanford F.C., Carmine B., Misra M. Effects of Sleeve Gastrectomy on Bone Mar-row Adipose Tissue in Adolescents and Young Adults with Obesity. J. Clin. Endocrinol. Metab. 2020;105:e3961–e3970. doi: 10.1210/clinem/dgaa581. PubMed DOI PMC
Huber F.A., Singhal V., Tuli S., Becetti I., López López A.P., Bouxsein M.L., Misra M., Bredella M.A. Two-year Skeletal Effects of Sleeve Gastrectomy in Ado-lescents with Obesity Assessed with Quantitative CT and MR Spectroscopy. Radiology. 2023;307:e223256. doi: 10.1148/radiol.223256. PubMed DOI PMC
Bredella M.A., Greenblatt L.B., Eajazi A., Torriani M., Yu E.W. Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue. Bone. 2017;95:85–90. doi: 10.1016/j.bone.2016.11.014. PubMed DOI PMC
Ivaska K.K., Huovinen V., Soinio M., Hannukainen J.C., Saunavaara V., Salminen P., Helmiö M., Parkkola R., Nuutila P., Kiviranta R. Changes in bone metabolism after bariatric surgery by gastric bypass or sleeve gastrectomy. Bone. 2017;95:47–54. doi: 10.1016/j.bone.2016.11.001. PubMed DOI
Rao R.S., Rao V., Kini S. Animal models in bariatric surgery—A review of the surgical techniques and postsurgical physiology. Obes. Surg. 2010;20:1293–1305. doi: 10.1007/s11695-010-0135-x. PubMed DOI
Lutz T.A., Bueter M. The Use of Rat and Mouse Models in Bariatric Surgery Experiments. Front. Nutr. 2016;3:25. doi: 10.3389/fnut.2016.00025. PubMed DOI PMC
Scheller E.L., Doucette C.R., Learman B.S., Cawthorn W.P., Khandaker S., Schell B., Wu B., Ding S.-Y., Bredella M.A., Fazeli P.K., et al. Region-specific variation in the properties of skeletal adipocytes reveals regulated and constitutive marrow adipose tissues. Nat. Commun. 2015;6:7808. doi: 10.1038/ncomms8808. PubMed DOI PMC
Li Z., Hardij J., Bagchi D.P., Scheller E.L., MacDougald O.A. Development, regulation, metabolism and function of bone marrow adipose tissues. Bone. 2018;110:134–140. doi: 10.1016/j.bone.2018.01.008. PubMed DOI PMC
Suchacki K.J., Cawthorn W.P. Molecular Interaction of Bone Marrow Adipose Tissue with Energy Metabolism. Curr. Mol. Biol. Rep. 2018;4:41–49. doi: 10.1007/s40610-018-0096-8. PubMed DOI PMC
Scheller E.L., Khandaker S., Learman B.S., Cawthorn W.P., Anderson L.M., Pham H., Robles H., Wang Z., Li Z., Parlee S.D., et al. Bone marrow adipocytes resist lipolysis and remodeling in response to β-adrenergic stimulation. Bone. 2019;118:32–41. doi: 10.1016/j.bone.2018.01.016. PubMed DOI PMC
Styner M., Thompson W.R., Galior K., Uzer G., Wu X., Kadari S., Case N., Xie Z., Sen B., Romaine A., et al. Bone marrow fat accumulation accelerated by high fat diet is suppressed by exercise. Bone. 2014;64:39–46. doi: 10.1016/j.bone.2014.03.044. PubMed DOI PMC
Li Z., Hardij J., Evers S.S., Hutch C.R., Choi S.M., Shao Y., Learman B.S., Lewis K.T., Schill R.L., Mori H., et al. G-CSF partially mediates effects of sleeve gastrectomy on the bone marrow niche. J. Clin. Investig. 2019;129:2404–2416. doi: 10.1172/JCI126173. PubMed DOI PMC
Bozadjieva-Kramer N., Shin J.H., Shao Y., Gutierrez-Aguilar R., Li Z., Heppner K.M., Chiang S., Vargo S.G., Granger K., Sandoval D.A., et al. Intestinal-derived FGF15 protects against deleterious effects of vertical sleeve gastrectomy in mice. Nat. Commun. 2021;12:4768. doi: 10.1038/s41467-021-24914-y. PubMed DOI PMC
Fazeli P.K., Horowitz M.C., MacDougald O.A., Scheller E.L., Rodeheffer M.S., Rosen C.J., Klibanski A. Marrow fat and bone—New perspectives. J. Clin. Endocrinol. Metab. 2013;98:935–945. doi: 10.1210/jc.2012-3634. PubMed DOI PMC
Botolin S., McCabe L.R. Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology. 2007;148:198–205. doi: 10.1210/en.2006-1006. PubMed DOI
Sulston R.J., Learman B.S., Zhang B., Scheller E.L., Parlee S.D., Simon B.R., Mori H., Bree A.J., Wallace R.J., Krishnan V., et al. Increased Circulating Adiponectin in Response to Thiazolidinediones: Investigating the Role of Bone Marrow Adipose Tissue. Front. Endocrinol. 2016;7:128. doi: 10.3389/fendo.2016.00128. PubMed DOI PMC
Tencerova M., Figeac F., Ditzel N., Taipaleenmäki H., Nielsen T.K., Kassem M. High-Fat Diet-Induced Obesity Promotes Expansion of Bone Marrow Adipose Tissue and Impairs Skeletal Stem Cell Functions in Mice. J. Bone Miner. Res. 2018;33:1154–1165. doi: 10.1002/jbmr.3408. PubMed DOI
Devlin M.J., Cloutier A.M., Thomas N.A., Panus D.A., Lotinun S., Pinz I., Baron R., Rosen C.J., Bouxsein M.L. Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J. Bone Miner. Res. 2010;25:2078–2088. doi: 10.1002/jbmr.82. PubMed DOI PMC
Cawthorn W.P., Scheller E.L., Parlee S.D., Pham H.A., Learman B.S., Redshaw C.M.H., Sulston R.J., Burr A.A., Das A.K., Simon B.R., et al. Expansion of Bone Marrow Adipose Tissue During Caloric Restriction Is Associated With Increased Circulating Glucocorticoids and Not With Hypoleptinemia. Endocrinology. 2016;157:508–521. doi: 10.1210/en.2015-1477. PubMed DOI PMC
Li Z., Bagchi D.P., Zhu J., Bowers E., Yu H., Hardij J., Mori H., Granger K., Skjaerlund J.D., Mandair G.S., et al. Constitutive bone marrow adipocytes suppress local bone formation. J. Clin. Investig. 2022;7:e160915. doi: 10.1172/jci.insight.160915. PubMed DOI PMC
Baum T., Yap S.P., Karampinos D.C., Nardo L., Kuo D., Burghardt A.J., Masharani U.B., Schwartz A.V., Li X., Link T.M. Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine bone mineral density, and blood biomarkers in women with type 2 diabetes mellitus? J. Magn. Reason. Imaging. 2012;35:117–124. doi: 10.1002/jmri.22757. PubMed DOI PMC
Sheu Y., Amati F., Schwartz A.V., Danielson M.E., Li X., Boudreau R., Cauley J.A., Osteoporotic Fractures in Men (MrOS) Research Group Vertebral bone marrow fat, bone mineral density and diabetes: The Osteoporotic Fractures in Men (MrOS) study. Bone. 2017;97:299–305. doi: 10.1016/j.bone.2017.02.001. PubMed DOI PMC
Yu E.W., Greenblatt L., Eajazi A., Torriani M., Bredella M.A. Marrow adipose tissue composition in adults with morbid obesity. Bone. 2017;97:38–42. doi: 10.1016/j.bone.2016.12.018. PubMed DOI PMC
Woods G.N., Ewing S.K., Sigurdsson S., Kado D.M., Ix J.H., Hue T.F., Eiriksdottir G., Xu K., Gudnason V., Lang T.F., et al. Chronic Kidney Disease Is Associated with Greater Bone Marrow Adiposity. J. Bone Miner. Res. 2018;33:2158–2164. doi: 10.1002/jbmr.3562. PubMed DOI PMC
Moorthi R.N., Fadel W., Eckert G.J., Ponsler-Sipes K., Moe S.M., Lin C. Bone marrow fat is increased in chronic kidney disease by magnetic resonance spectroscopy. Osteoporos. Int. 2015;26:1801–1807. doi: 10.1007/s00198-015-3064-7. PubMed DOI PMC
Badr S., Cotten A., Mentaverri R., Lombardo D., Labreuche J., Martin C., Hénaut L., Cortet B., Paccou J. Relationship between Bone Marrow Adipose Tissue and kidney function in postmenopausal women. Bone Rep. 2023;19:101713. doi: 10.1016/j.bonr.2023.101713. PubMed DOI PMC
Kuiper J.W., van Kuijk C., Grashuis J.L., Ederveen A.G.H., Schütte H.E. Accuracy and the Influence of Marrow Fat on Quantitative CT and Dual-Energy X-ray Absorp-tiometry Measurements of the Femoral Neck in Vitro. Osteoporos. Int. 1996;6:25–30. doi: 10.1007/BF01626534. PubMed DOI
Sfeir J.G., Drake M.T., Atkinson E.J., Achenbach S.J., Camp J.J., Tweed A.J., McCready L.K., Yu L., Adkins M.C., Amin S., et al. Evaluation of Cross-Sectional and Longitudinal Changes in Volumetric Bone Mineral Density in Postmenopausal Women Using Single-versus Dual-Energy Quantitative Computed Tomography. Bone. 2018;112:145–152. doi: 10.1016/j.bone.2018.04.023. PubMed DOI PMC
Yu E.W., Thomas B.J., Brown J.K., Finkelstein J.S. Simulated Increases in Body Fat and Errors in Bone Mineral Density Measurements by DXA and QCT. J. Bone Miner. Res. 2012;27:119–124. doi: 10.1002/jbmr.506. PubMed DOI PMC