The pathophysiology of osteoporosis in obesity and type 2 diabetes in aging women and men: The mechanisms and roles of increased bone marrow adiposity
Open accessAbstract
Osteoporosis is defined as a systemic skeletal disease characterized by decreased bone mass and micro-architectural deterioration leading to increased fracture risk. Osteoporosis incidence increases with age in both post-menopausal women and aging men. Among other important contributing factors to bone fragility observed in osteoporosis, that also affect the elderly population, are metabolic disturbances observed in obesity and Type 2 Diabetes (T2D). These metabolic complications are associated with impaired bone homeostasis and a higher fracture risk. Expansion of the Bone Marrow Adipose Tissue (BMAT), at the expense of decreased bone formation, is thought to be one of the key pathogenic mechanisms underlying osteoporosis and bone fragility in obesity and T2D. Our review provides a summary of mechanisms behind increased Bone Marrow Adiposity (BMA) during aging and highlights the pre-clinical and clinical studies connecting obesity and T2D, to BMA and bone fragility in aging osteoporotic women and men.
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AD mice at a younger age recapitulate an aged skeletal phenotype.
“As aging-related osteoporosis typically features low bone mass, microarchitectural alterations and bone marrow adipose tissue expansion40–42, our findings suggest that AD mice at a younger age recapitulate an aged skeletal phenotype.”
From Serum amyloid P secreted by bone marrow adipocytes drives skeletal amyloidosis (2025) · cites this paper as [40]
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BackgroundSelf-citationWeivoda, M. M., Chew, C. K., Monroe, D. G., Farr, J. N., Atkinson, E. J., Geske, J. R., Eckhardt, B., Thicke, B., Ruan, M., Tweed, A. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-14003-6 · Cited by 230 · see citing works
Self-citationObesity, Type 2 Diabetes and Bone in Adults
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“Frontiers in Endocrinology 05 BMAT formation evaluated by measurement of BMAT volume, BMAd size and number (70, 92–98), which was correlated with increased, unchanged, or decreased BMD in mice depending on the employed diabetic model (T1D or T2D) (70, 71, 94, 95, 99), but associated with a higher risk of fractures.”
MethodSenescence‐associated intrinsic mechanisms of osteoblast dysfunctions
Kassem, M., & Marie, P. (2011) · Aging Cell · doi:10.1111/j.1474-9726.2011.00669.x · Cited by 228 · cited 1× · see citing works
“Osteoporosis is primarily attributed to aging and sex-steroid deficiency, which at the cellular level leads to increased bone resorption by osteoclasts and decreased bone formation by osteoblasts (6, 7).”
BackgroundSelf-citationGreco, E., Fornari, R., Rossi, F., Santiemma, V., Prossomariti, G., Annoscia, C., Aversa, A., Brama, M., Marini, M., Donini, L., et al. (2010) · International journal of clinical practice · doi:10.1111/j.1742-1241.2009.02301.x · Cited by 228 · see citing works
Baum, T. H., Yap, S. P., Karampinos, D. C., Nardo, L., Kuo, D. Z., Burghardt, A. J., Masharani, U. B., Schwartz, A. V., Li, X., & Link, T. M. (2011) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22757 · Cited by 227 · see citing works
Kajkenova, O., Lecka‐Czernik, B., Gubrij, I. B., Hauser, S. P., Takahashi, K., PARFITT, A. M., Jilka, R. L., Manolagas, S. C., & Lipschitz, D. A. (1997) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1997.12.11.1772 · Cited by 226 · cited 1× · see citing works
“microenvironment, leading to compromised bone formation and decreased bone mass (30).”
BackgroundBone marrow fat content in the elderly: A reversal of sex difference seen in younger subjects
Griffith, J., Yeung, D., Ma, H. T., Leung, J., Kwok, T., & Leung, P. (2012) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.23619 · Cited by 226 · cited 2× · see citing works
“Frontiers in Endocrinology 04 An interesting question that has been raised is whether the biological sex has an impact on the expansion of BMAT during aging? Griffith et al, investigated BMD and BMAT in the lumbar spine of 259 healthy subjects (145 females, 114 males; age range: 62-90 years) using MR spectroscopy of L…”
BackgroundMethodGoulding, A., & Taylor, R. (1998) · Calcified Tissue International · doi:10.1007/s002239900557 · Cited by 220 · see citing works
Tencerova, M., Figeac, F., Ditzel, N., Taipaleenmäki, H., Nielsen, T., & Kassem, M. (2018) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3408 · Cited by 218 · cited 4× · see citing works
“Frontiers in Endocrinology 05 BMAT formation evaluated by measurement of BMAT volume, BMAd size and number (70, 92–98), which was correlated with increased, unchanged, or decreased BMD in mice depending on the employed diabetic model (T1D or T2D) (70, 71, 94, 95, 99), but associated with a higher risk of fractures.”
BackgroundMethodInfluentialSelf-citationBaxter-Jones, A., Kontulainen, S., Faulkner, R., & Bailey, D. (2008) · Bone · doi:10.1016/j.bone.2008.07.245 · Cited by 213 · see citing works
Harrison, S. A., Alkhouri, N., Davison, B. A., Sanyal, A., Edwards, C., Colca, J. R., Lee, B. H., Loomba, R., Cusi, K., Kolterman, O., et al. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2019.10.023 · Cited by 211 · see citing works
Antiresorptive therapies for osteoporosis: a clinical overview
Chen, J. S., & Sambrook, P. N. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.146 · Cited by 209 · see citing works
Effects of estrogen therapy on bone marrow adipocytes in postmenopausal osteoporotic women
Syed, F., Oursler, M., Hefferanm, T. E., Peterson, J., Riggs, B., & Khosla, S. (2008) · Osteoporosis International · doi:10.1007/s00198-008-0574-6 · Cited by 207 · see citing works
Cohen, A., Dempster, D. W., Recker, R. R., Lappe, J. M., Zhou, H., Zwahlen, A., Müller, R., Zhao, B., Guo, X., Lang, T., et al. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1047 · Cited by 206 · cited 1× · see citing works
“Along with this finding, several clinical studies including ours have noted reduced bone turnover in patients with metabolic diseases (71, 103).”
ResultRauch, A., Haakonsson, A., Madsen, J., Larsen, M., Forss, I., Madsen, M. R., Hauwaert, E. L. V., Wiwie, C., Jespersen, N., Tencerova, M., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0359-1 · Cited by 202 · cited 1× · see citing works
“Comprehensive characterization of the epigenomic and transcriptional changes associated with osteoblast and adipocyte differentiation of BMSCs has shown that the inverse correlation between fate specification of BMSCs into osteoblast versus adipocyte lineages is regulated by a large and diverse network of transcriptio…”
BackgroundSelf-citationThe Role and Mechanism of SIRT1 in Resveratrol-regulated Osteoblast Autophagy in Osteoporosis Rats
Yang, X., Jiang, T., Wang, Y., & Guo, L. (2019) · Scientific Reports · doi:10.1038/s41598-019-44766-3 · Cited by 201 · see citing works
Bone Fractures and Hypoglycemic Treatment in Type 2 Diabetic Patients
Monami, M., Cresci, B., Colombini, A., Pala, L., Balzi, D., Gori, F., Chiasserini, V., Marchionni, N., Rotella, C. M., & Mannucci, E. (2008) · Diabetes Care · doi:10.2337/dc07-1736 · Cited by 194 · see citing works
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“BMSCs obtained from old mice also exhibited increased expression of SASP markers, leading to increased osteoclast formation, as well as increased expression of the adipogenic transcription factor PPAR-g (45).”
BackgroundObesity in menopause - our negligence or an unfortunate inevitability
Kozakowski, J., Gietka-Czernel, M., Leszczyńska, D., & Majos, A. (2017) · Menopausal Review · doi:10.5114/pm.2017.68594 · Cited by 189 · see citing works
The Role of Vitamin D in the Aging Adult
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State of the art in osteoporosis risk assessment and treatment
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“Fractures, due to osteoporosis, require hospitalization and increase risk of mortality by 20%, and in 50% of the cases, result in chronic disability (3).”
BackgroundRibot, C., Trémollières, F., Pouilles, J., Bonneu, M., Germain, F., & Louvet, J. (1987) · Bone · doi:10.1016/8756-3282(87)90062-7 · Cited by 187 · cited 1× · see citing works
“In addition, it is shown that lumbar spine BMD is inversely associated with the lumbar adiposity in adults with morbid obesity, and that morbid obesity and T2D exhibits a higher BMA than nondiabetic controls of similar weight (98).”
BackgroundHigh Fat Diet-Induced Animal Model of Age-associated Obesity and Osteoporosis
Halade, G., Rahman, M. M., Williams, P., & Fernandes, G. (2010) · Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.10.002 · Cited by 186 · cited 2× · see citing works
“Another question that has been raised recently is whether gender-affirming interventions have an impact on bone microstructure and BMA? Gender-affirming interventions using hormone therapy or surgery aim to align the physical characteristics with an individual’s gender identity (85).”
BackgroundFOXP1 controls mesenchymal stem cell commitment and senescence during skeletal aging
Li, H., Liu, P., Xu, S., Li, Y., Dekker, J. D., Li, B., Fan, Y., Zhang, Z., Hong, Y., Yang, G., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci89511 · Cited by 180 · cited 1× · see citing works
“Mouse genetic studies had shown that conditional depletion of Foxp1 in BMSCs leads to premature aging, bone loss, and increased BMA via Foxp1 interactions with different members of C/EBP family proteins, such as C/EBP b/d, which are key modulators of adipogenesis (38).”
BackgroundZinman, B., Haffner, S. M., Herman, W. H., Holman, R. R., Lachin, J. M., Kravitz, B. G., Paul, G., Jones, N. C., Aftring, R. P., Viberti, G. C., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0572 · Cited by 180 · see citing works
Dipeptidyl Peptidase-4 Inhibitors and Bone Fractures
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McColm, J., Hu, L.-J., Womack, T., Tang, C.-C., & Chiang, A. Y. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2092 · Cited by 173 · see citing works
Editorial: Cytokines, Estrogen, and Postmenopausal Osteoporosis-The Second Decade.
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“Changes in BMA during aging in males and females 145 females, 114 males; age range (62-90) years.”
BackgroundBone quality changes associated with aging and disease: a review
Boskey, A., & Imbert, L. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13572 · Cited by 163 · see citing works
Doucette, C. R., Horowitz, M., Berry, R., MacDougald, O., Anunciado-Koza, R., Koza, R. A., & Rosen, C. J. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.24954 · Cited by 163 · cited 2× · see citing works
“Changes in BMA during aging in males and females 145 females, 114 males; age range (62-90) years.”
BackgroundMethodCigarette smoking, obesity, and bone mass
Slemenda, C., Hui, S., Longcope, C., & Johnston, C. C. (1989) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650040513 · Cited by 162 · see citing works
Alendronate Has an Anabolic Effect on Bone Through the Differentiation of Mesenchymal Stem Cells
Duque, G., & Rivas, D. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.070701 · Cited by 156 · see citing works
Calcium Supplementation Suppresses Bone Turnover During Weight Reduction in Postmenopausal Women
Ricci, T. A., Chowdhury, H., Heymsfield, S., Stahl, T. J., Pierson, R. N., & Shapses, S. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.6.1045 · Cited by 155 · see citing works
Direct and Indirect Estrogen Actions on Osteoblasts and Osteoclasts
Zallone, A. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1346.019 · Cited by 150 · cited 1× · see citing works
“Changes in BMA during aging in males and females 145 females, 114 males; age range (62-90) years.”
BackgroundYamaguchi, T., Kanazawa, I., Yamamoto, M., Kurioka, S., Yamauchi, M., Yano, S., & Sugimoto, T. (2009) · Bone · doi:10.1016/j.bone.2009.05.003 · Cited by 145 · see citing works
The Bones of Children With Obesity
Fintini, D., Cianfarani, S., Cofini, M., Andreoletti, A., Ubertini, G., Cappa, M., & Manco, M. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00200 · Cited by 143 · see citing works
Lecka-Czernik, B., Stechschulte, L. A., Czernik, P., & Dowling, A. R. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.01.001 · Cited by 141 · cited 1× · see citing works
“Changes in BMA during aging in males and females 145 females, 114 males; age range (62-90) years.”
BackgroundThe skeletal cell‐derived molecule sclerostin drives bone marrow adipogenesis
Fairfield, H. E., Falank, C. R., Harris, E., DeMambro, V., McDonald, M. M., Pettitt, J. A., Mohanty, S. T., Croucher, P. I., Krämer, I., Kneissel, M., et al. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25976 · Cited by 140 · see citing works
Is obesity in women protective against osteoporosis?
Migliaccio, S., Greco, E. A., Fornari, F., Donini, L. M., & Lenzi (2011) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s11920 · Cited by 137 · see citing works
Changes 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 · cited 2× · see citing works
“showed lower bone mass acquisition and greater increases in BMAT indices in Transgender and Gender Non-Conforming (TGNC) youth after 12 months of pubertal suppression with gonadotropin-releasing hormone agonists (87).”
BackgroundEbeling, P. R. (2013) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e328362164d · Cited by 127 · cited 1× · see citing works
“Gradual reduction in the testosterone levels in aging men are associated with reduction in bone mass (60, 61), and osteoblast dysfunction (62).”
BackgroundAlmeida, M., Martín-Millán, M., Ambrogini, E., Bradsher, R., Han, L., Chen, X.-D., Roberson, P., Weinstein, R., O'Brien, C. A., Jilka, R., et al. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.091017 · Cited by 126 · cited 1× · see citing works
“Estrogen is involved in molecular signaling in bone and regulation of BMAds (53–55) as estrogen is a positive regulator of osteogenesis through activation of estrogen receptor (ER)-dependent cytoplasmic kinases, BMPs and Wnt signaling (56, 57).”
BackgroundKelly, K. A., & Gimble, J. (1998) · Endocrinology · doi:10.1210/endo.139.5.5970 · Cited by 126
Tencerova, M., Frost, M., Figeac, F., Nielsen, T., Ali, D., Lauterlein, J., Andersen, T. L., Haakonsson, A., Rauch, A., Madsen, J. S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.066 · Cited by 125 · cited 7× · see citing works
“Along with this finding, several clinical studies including ours have noted reduced bone turnover in patients with metabolic diseases (71, 103).”
BackgroundMethodResultInfluentialSelf-citationHamann, C., Rauner, M., Höhna, Y., Bernhardt, R., Mettelsiefen, J., Goettsch, C., Günther, K., Stolina, M., Han, C.-Y. E., Asuncion, F., et al. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1803 · Cited by 120 · see citing works
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“A number of underlying pathogenic mechanisms of osteoporosis have been proposed, such as estrogen deficiency-associated Bone Marrow (BM) inflammation (8) or decreased levels of anabolic hormones (9, 10).”
BackgroundThe interrelationship between bone and fat: from cellular see-saw to endocrine reciprocity
Gijsen, H. S., Crowther, N. J., Hough, F. S., & Ferris, W. F. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1211-2 · Cited by 113 · see citing works
Effect of estrogens on bone marrow adipogenesis and Sirt1 in aging C57BL/6J mice
Elbaz, A., Rivas, D., & Duque, G. (2009) · Biogerontology (Dordrecht) · doi:10.1007/s10522-009-9221-7 · Cited by 111 · see citing works
Chandra, A., Lin, T., Young, T. J., Tong, W., Ma, X., Tseng, W., Krämer, I., Kneissel, M., Levine, M. A., Zhang, Y., et al. (2016) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2996 · Cited by 110 · see citing works
The Role of Oxidative Stress in the Development of Diabetes Mellitus and Its Complications
dos Santos, J. D., Tewari, S., & Mendes, R. (2019) · Journal of Diabetes Research · doi:10.1155/2019/4189813 · Cited by 110
Suen, P. K., & Qin, L. (2015) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2015.08.004 · Cited by 107 · see citing works
Factors affecting bone mineral density in postmenopausal women
Heidari, B., Hosseini, R., Javadian, Y., Bijani, A., Sateri, M. H., & Nouroddini, H. G. (2015) · Archives of Osteoporosis · doi:10.1007/s11657-015-0217-4 · Cited by 104 · see citing works
Association between Obesity and Bone Mineral Density by Gender and Menopausal Status
Salamat, M. R., Salamat, A. H., & Janghorbani, M. (2016) · Endocrinology and Metabolism · doi:10.3803/enm.2016.31.4.547 · Cited by 103 · see citing works
Exercise Decreases Marrow Adipose Tissue Through ß-Oxidation in Obese Running Mice
Styner, M., Pagnotti, G. M., McGrath, C., Wu, X., Sen, B., Uzer, G., Xie, Z., Zong, X., Styner, M. A., Rubin, C. T., et al. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3159 · Cited by 100 · see citing works
The role of insulin-like growth factor I components in the regulation of vitamin D
Manuel Gomez, J. (2006) · Current Pharmaceutical Biotechnology · doi:10.2174/138920106776597621 · Cited by 96 · see citing works
Marrow adipose tissue composition in adults with morbid obesity
Yu, E. W., Greenblatt, L. B., Eajazi, A., Torriani, M., & Bredella, M. (2016) · Bone · doi:10.1016/j.bone.2016.12.018 · Cited by 96 · cited 2× · see citing works
“Osteoporosis and aging are characterized with decreased BMD, along with increased BMAT and accompanied by increased resorption activity in the BM in mice and humans (90, 91).”
BackgroundMaddalozzo, G., Turner, R. T., Edwards, C., Howe, K., Widrick, J., Rosen, C. J., & Iwaniec, U. (2009) · Osteoporosis International · doi:10.1007/s00198-009-0836-y · Cited by 96 · see citing works
Ameri, P., Giusti, A., Boschetti, M., Bovio, M., Teti, C., Leoncini, G., Ferone, D., Murialdo, G., & Minuto, F. (2013) · European Journal of Endocrinology · doi:10.1530/eje-13-0510 · Cited by 95 · see citing works
Prakasam, G., Yeh, J. K., Chen, M. M., Castro-Magaña, M., Liang, C. T., & Aloia, J. F. (1999) · Bone · doi:10.1016/s8756-3282(99)00018-6 · Cited by 94 · cited 1× · see citing works
“Testosterone exhibits an anabolic impact on bone formation in the periosteal surface in mice (58), and that oral administration of testosterone reduces the accelerated bone loss in orchiectomized mice (59).”
BackgroundMarie, P., Sabbagh, A., de Vernejoul, M., & Lomri, A. (1989) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jcem-69-2-272 · Cited by 93 · cited 2×
“increased bone resorption and bone formation, manifested by increased number of osteoblast precursors, osteoblast proliferation and increased osteoblast number (72, 73).”
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Marie, P. J., de Vernejoul, M., Connes, D., & Hott, M. (1991) · Journal of Clinical Investigation · doi:10.1172/jci115418 · Cited by 87 · cited 2× · see citing works
“Gradual reduction in the testosterone levels in aging men are associated with reduction in bone mass (60, 61), and osteoblast dysfunction (62).”
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“Estrogen is involved in molecular signaling in bone and regulation of BMAds (53–55) as estrogen is a positive regulator of osteogenesis through activation of estrogen receptor (ER)-dependent cytoplasmic kinases, BMPs and Wnt signaling (56, 57).”
BackgroundPPARG Post-translational Modifications Regulate Bone Formation and Bone Resorption
Stechschulte, L. A., Czernik, P., Rotter, Z. C., Tausif, F. N., Corzo, C. A., Marciano, D., Asteian, A., Zheng, J., Bruning, J., Kamenecka, T., et al. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.06.040 · Cited by 85 · see citing works
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Martin, R. B., Chow, B. D., & Lucas, P. A. (1990) · Calcified Tissue International · doi:10.1007/bf02555043 · Cited by 85 · see citing works
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Early-onset type 2 diabetes impairs skeletal acquisition in the male TALLYHO/JngJ mouse.
Devlin, M. J., van Vliet, M., Motyl, K., Karim, L., Brooks, D. J., Louis, L., Conlon, C., Rosen, C., & Bouxsein, M. (2014) · Endocrinology · doi:10.1210/en.2014-1041 · Cited by 82 · see citing works
Vitamin D endocrine system and osteoblasts.
van Driel, M., & van Leeuwen, J. (2014) · BoneKEy Reports · doi:10.1038/bonekey.2013.227 · Cited by 81 · see citing works
Bone Turnover Is Suppressed in Insulin Resistance, Independent of Adiposity
Tonks, K., White, C. P., J. Center, Samocha-Bonet, D., & Greenfield, J. (2017) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2016-3282 · Cited by 80 · cited 1× · see citing works
“Frontiers in Endocrinology 05 BMAT formation evaluated by measurement of BMAT volume, BMAd size and number (70, 92–98), which was correlated with increased, unchanged, or decreased BMD in mice depending on the employed diabetic model (T1D or T2D) (70, 71, 94, 95, 99), but associated with a higher risk of fractures.”
MethodShort‐Term Effect of Estrogen on Human Bone Marrow Fat
Limonard, E., Veldhuis-Vlug, A., van Dussen, L., Runge, J., Tanck, M. W., Endert, E., Heijboer, A., Fliers, E., Hollak, C., Akkerman, E., et al. (2015) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2557 · Cited by 80 · see citing works
Sclerostin monoclonal antibody enhanced bone fracture healing in an open osteotomy model in rats
Suen, P.-K., He, Y.-X., Chow, D., Huang, L., Li, C., Ke, H., Ominsky, M., & Qin, L. (2014) · Journal of Orthopaedic Research · doi:10.1002/jor.22636 · Cited by 78 · see citing works
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The Effects of Adiponectin and Leptin on Changes in Bone Mineral Density
Barbour, K. E., Zmuda, J., Boudreau, R., Strotmeyer, E., Horwitz, M., Evans, R., Kanaya, A., Harris, T. B., & Cauley, J. (2011) · Osteoporosis International · doi:10.1007/s00198-011-1768-x · Cited by 77 · see citing works
Osteoporosis Treatment with Anti-Sclerostin Antibodies—Mechanisms of Action and Clinical Application
Rauner, M., Taipaleenmäki, H., Tsourdi, E. A., & Winter, E. M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10040787 · Cited by 77 · see citing works
Li, Y.-J., Lu, L., Xie, Y., Chen, X., Tian, L., Liang, Y., Li, H.-F., Zhang, J., Liu, Y., & Yu, X.-J. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.622950 · Cited by 76 · see citing works
Extrinsic Mechanisms Involved in Age-Related Defective Bone Formation
Marie, P. J., & Kassem, M. S. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2113 · Cited by 76 · cited 1× · see citing works
“leading to inhibited bone formation and enhanced bone resorption (48).”
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Sclerostin Antibody Treatment Improves Fracture Outcomes in a Type I Diabetic Mouse Model
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The implications of bone marrow adipose tissue on inflammaging
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“Aging, osteoporosis and metabolic diseases such as obesity and diabetes robustly affect microstructural changes in the BM and contribute to impairment of bone homeostasis, which leads to higher risk of bone fractures (88, 89).”
BackgroundDLK1 is a novel regulator of bone mass that mediates estrogen deficiency–induced bone loss in mice
Abdallah, B., Ditzel, N., Mahmood, A., Isa, A., Traustadottir, G. A., Schilling, A., Ruiz-Hidalgo, M., Laborda, J., Amling, M., & Kassem, M. (2011) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.346 · Cited by 71 · see citing works
Self-citationInfluence of obesity on bone density in postmenopausal women.
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“IL-6 is one of the cytokines that is secreted by BMAds and increases osteoclast formation and bone resorption, thereby leading to decreased BMD in men and women (150, 151).”
BackgroundResultInfluentialSelf-citationBone damage in type 2 diabetes mellitus.
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Self-citationBone marrow fat changes after gastric bypass surgery are associated with loss of bone mass
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“Testosterone exhibits an anabolic impact on bone formation in the periosteal surface in mice (58), and that oral administration of testosterone reduces the accelerated bone loss in orchiectomized mice (59).”
BackgroundAdiponectin is associated with low bone mineral density in elderly men.
Basurto, L., Galván, R., Córdova, N., Saucedo, R., Vargas, C., Campos, S., Halley, E., Avelar, F., & Zarate, A. (2008) · European Journal of Endocrinology · doi:10.1530/eje-08-0569 · Cited by 65 · see citing works
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Insulin-Dependent Adipogenesis in Stromal ST2 Cells Derived from Murine Bone Marrow
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Metformin prevents anti-osteogenic in vivo and ex vivo effects of rosiglitazone in rats.
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Greater Bone Marrow Adiposity Predicts Bone Loss in Older Women
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“2) years BMA is associated with higher loss of trabecular bone at the spine area and femoral neck, and greater loss of spine strength (75)”
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Targeting the Androgen Receptor
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“In addition, in vivo murine studies using irradiation or physiological aging models, in which increased levels of ROS within the bone microenvironment are associated with expansion of BMAT and compromised skeletal homeostasis, indicated that antioxidant agents Dasatinib and Quercetin reduced BMAT and enhanced bone for…”
BackgroundInfluentialFigeac, F., Tencerova, M., Ali, D., Andersen, T. L., Appadoo, D. R. C., Kerckhofs, G., Ditzel, N., Kowal, J., Rauch, A., & Kassem, M. (2022) · Stem Cells · doi:10.1093/stmcls/sxab011 · Cited by 50 · see citing works
Self-citationThe dynamics of human bone marrow adipose tissue in response to feeding and fasting
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“Frontiers in Endocrinology 05 BMAT formation evaluated by measurement of BMAT volume, BMAd size and number (70, 92–98), which was correlated with increased, unchanged, or decreased BMD in mice depending on the employed diabetic model (T1D or T2D) (70, 71, 94, 95, 99), but associated with a higher risk of fractures.”
MethodAndrogens as anabolic agents for bone
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“Gradual reduction in the testosterone levels in aging men are associated with reduction in bone mass (60, 61), and osteoblast dysfunction (62).”
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“Human studies had shown that expansion of visceral fat is associated with enhanced adipocyte formation in the BM microenvironment in osteoporotic obese women (97).”
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An Insulin-Sensitizing Thiazolidinedione, Which Minimally Activates PPARγ, Does Not Cause Bone Loss
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Marrow Fat-Secreted Factors as Biomarkers for Osteoporosis
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Links among Obesity, Type 2 Diabetes Mellitus, and Osteoporosis: Bone as a Target
Martiniaková, M., Bíro, R., Pénzes, N., Šarocká, A., Kováčová, V., Mondočková, V., & Omelka, R. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094827 · Cited by 94 · see citing works
“More than 30 million people in Europe are expected to be affected by osteoporosis by 2050 [7–9].”
BackgroundInfluentialThe multi-faceted nature of age-associated osteoporosis
Smit, A. E., Meijer, O. C., & Winter, E. M. (2024) · Bone Reports · doi:10.1016/j.bonr.2024.101750 · Cited by 72 · see citing works
“In addition, several disorders that are associated with age, such as diabetes mellitus (DM) and obesity, both induce bone marrow adipogenesis and reduce bone formation (Ali et al., 2022).”
BackgroundObesity and lipid metabolism in the development of osteoporosis (Review)
Wang, X., Zhang, C., Zhao, G.-T., Yang, K., & Tao, L. (2024) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2024.5385 · Cited by 70 · see citing works
“Based on the balance of osteo‑ genesis and adipogenesis, the expansion of bone marrow adipose tissue is common in populations at a high risk for osteoporosis, leading to decreased bone formation (24).”
BackgroundZhang, Y.-S., He, X., Wang, K., Xue, Y., Hu, S.-H., Jin, Y.-S., Zhu, G., Rui, Y.-J., & Shi, Q. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.04.013 · Cited by 49 · see citing works
“Accumulating evidence affirms that obesity is deeply involved in osteoporosis [35]; however, its relevant mechanism should be strongly emphasized.”
Endocrinal metabolic regulation on the skeletal system in post-menopausal women
Thapa, S., Nandy, A., & Rendina-Ruedy, E. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1052429 · Cited by 49 · see citing works
“, 2009), as well as during obesity (Elia, 2012; Rinonapoli et al., 2021; Ali et al., 2022).”
BackgroundBone health in adults with obesity before and after interventions to promote weight loss.
Paccou, J., & Compston, J. (2024) · The Lancet Diabetes and Endocrinology · doi:10.1016/s2213-8587(24)00163-3 · Cited by 38 · see citing works
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“This ‘fattening’ of bone, coupled with reduced bone formation, decreases trabecular bone density, resulting in a higher risk for fractures [126].”
BackgroundTrabecular Bone Score (TBS) in Individuals with Type 2 Diabetes Mellitus: An Updated Review
Trandafir, A., Sima, O.-C., Gheorghe, A., Ciuche, A., Cucu, A.-P., Nistor, C., & Carsote, M. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12237399 · Cited by 29 · see citing works
“…contributing to the risk of fracture in T2DM, diabetic bone disease representing a major co-morbidity as part of an already complicated panel, [17–19], noting once again the role of understanding and studding the bone fragility in T2DM due to the increased burden in terms of morbidity and even…”
BackgroundDeep learning and genome-wide association meta-analyses of bone marrow adiposity in the UK Biobank
Xu, W., Mesa-Eguiagaray, I., Morris, D. M., Wang, C.-J., Gray, C. D., Sjöström, S., Papanastasiou, G., Badr, S., Paccou, J., Li, X., et al. (2025) · Nature Communications · doi:10.1038/s41467-024-55422-4 · Cited by 25 · see citing works
“We alsoperformed Sex x Genotype interaction analysis, which did not fi nd P-sex genome-wide signi fi cant for any of the lead SNPs in four bone regions (Supplementary Data 53).”
Cai, G., Song, X., Luo, H., Dai, G.-Y., Zhang, H., Jiang, D., Lei, X., Chen, H., & Zhang, L.-W. (2024) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2024.112382 · Cited by 23 · see citing works
Common Regulators of Lipid Metabolism and Bone Marrow Adiposity in Postmenopausal Women
Kim, D.-Y., & Ko, S. (2023) · Pharmaceuticals · doi:10.3390/ph16020322 · Cited by 19 · see citing works
“Taken together, the loss of E2 is associated with rapid bone loss, osteoporosis, and an increased risk of fracture [93] as well as an increased BMA, as demonstrated by animal studies [11,83].”
BackgroundWang, K., Zhao, X., Yang, S., Qi, X., Li, A., & Yu, W. (2024) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.13374 · Cited by 17 · see citing works
Serum amyloid P secreted by bone marrow adipocytes drives skeletal amyloidosis
Kumar, S., Song, K., Wang, J., Baghel, M. S., Zeng, Y., Shen, K., Zheng, J., Crane, J., Demehri, S., Gao, P., et al. (2025) · Nature Aging · doi:10.1038/s43587-025-00924-z · Cited by 16 · see citing works
“Quantification by ELISA revealed increased human Aβ 1–40 and Aβ 1–42 levels in the bone marrow of AD mice compared to that of WT mice (Fig.”
Luo, W., Li, X.-Z., Zhou, Y., Xu, D., & Qiao, Y. (2024) · Scientific Reports · doi:10.1038/s41598-024-65571-7 · Cited by 16 · see citing works
Exploring the Interplay between Bone Marrow Stem Cells and Obesity
Moscatelli, F., Monda, A., Messina, G., Picciocchi, E., Monda, M., di Padova, M., Monda, V., Mezzogiorno, A., Dipace, A., Limone, P., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25052715 · Cited by 16 · see citing works
“Reduced endogenous antioxidant production is another effect of estrogen deficiency [37].”
BackgroundWang, L., Liu, Y.-D., Li, K., Zhang, W.-S., Yuan, Y., Ma, K.-K., Zhou, F.-Y., Cheng, Z.-T., Geng, J., Su, Y.-B., et al. (2024) · Obesity · doi:10.1002/oby.24040 · Cited by 13 · see citing works
“On the contrary, the response of BMAT to obesity is less clear, and some studies have reported no change or some increase in BMAT [26] depending on the diabetic status.”
BackgroundEmerzian, S. R., Johannesdottir, F., Yu, E. W., & Bouxsein, M. (2024) · JBMR Plus · doi:10.1093/jbmrpl/ziae003 · Cited by 13 · see citing works
“30,31 The aim of this review is to discuss the key findings from studies that have used noninvasive imaging to assess skeletal outcomes in adults with T1D and T2D.”
BackgroundTherapeutic applications of miRNA in the management of obesity and osteoporosis
Abolhasani, S., Ahmadi, Y., Rostami, Y., Zendeh, M. B., & Fattahi, D. (2025) · Journal of Diabetes and Metabolic Disorders · doi:10.1007/s40200-025-01589-6 · Cited by 12
“Therefore, the dual burden of obesity and osteoporosis can create a vicious cycle, wherein the presence of one condition exacerbates the other, leading to a heightened risk of fractures and other skeletal-related events [11].”
Guimarães, G. C., Coelho, J. B. C., Silva, J. G. O., de Sant’Ana, A. C. C., de Sá, C. A. C., Moreno, J. M., Reis, L. M., & Guimarães, C. S. D. O. (2023) · Osteoporosis International · doi:10.1007/s00198-023-06991-5 · Cited by 19 · see citing works
“Metabolic disturbances observed in obese and T2D patients contribute to BMAT expansion and bone fragility, both of which are considered underlying mechanisms involved in the pathogenesis of osteoporosis [81].”
Adipocyte–Tumor Interactions in the Bone Marrow Niche: Implications for Metastasis and Therapy
Dabaliz, A., Hakawati, M. N. A., Alrashdan, N., Alrashdan, S., Bakir, M., & Mohammad, K. S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26199781 · Cited by 11 · see citing works
“This shift contributes to bone fragility and osteoporosis [183].”
Bone marrow adipocytes provide early sign for progression from MGUS to multiple myeloma
El-Masri, B. M., Leka, B., Mustapha, F., Gundesen, M. T., Hinge, M., Lund, T., Andersen, T. L., Diaz‐delCastillo, M., & Jafari, A. (2024) · Oncotarget · doi:10.18632/oncotarget.28548 · Cited by 10 · see citing works
Self-citationTao, B., Shen, X.-M., Li, G.-F., Wu, X.-Y., Yang, Y., Sheng, C., Zhang, Y., Wang, L., Zhao, Z.-Y., Song, Q., et al. (2025) · Journal of Diabetes · doi:10.1111/1753-0407.70091 · Cited by 10
“These changes are directly associated with decreased bone mechanical performance and an increased fracture risk [15].”
Artificial intelligence–based diabetes risk prediction from longitudinal DXA bone measurements
Khan, S., & Shah, Z. (2025) · Scientific Reports · doi:10.1038/s41598-025-10136-5 · Cited by 9 · see citing works
KIAA1199 (CEMIP) regulates adipogenesis and whole-body energy metabolism
Chen, L., Shi, K., Ditzel, N., Qiu, W., Tencerová, M., Nielsen, L. H. D., Figeac, F., Rauch, A., Liu, Y., Tao, J., et al. (2025) · Bone Research · doi:10.1038/s41413-025-00415-2 · Cited by 9 · see citing works
“25 Under physiological conditions, BMAT is thought to provide energy needed for of bone remodeling and thus exhibits signi fi cant changes in metabolic bone diseases.”
Self-citationLeanza, G., Faraj, M., Cannata, F., Viola, V., Pellegrini, N., Tramontana, F., Pedone, C., Vadalà, G., Piccoli, A., Strollo, R., et al. (2026) · Metabolism · doi:10.1016/j.metabol.2026.156492 · Cited by 9 · see citing works
Cursano, M. C., Valsecchi, A. A., Pantano, F., Maïo, M. D., Procopio, G., Berruti, A., Bertoldo, F., Tucci, M., Giorgi, U. D., Santini, D., et al. (2024) · ESMO Open · doi:10.1016/j.esmoop.2024.103484 · Cited by 8 · see citing works
Ji, S.-J., Zhao, B., Gao, Y., Xie, J., Han, H., Wu, Q.-L., & Yang, D. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1367806 · Cited by 8
Materozzi, M., Resnati, M., Facchi, C., Trudu, M., Orfanelli, U., Perini, T., Gennari, L., Milan, E., & Cenci, S. (2024) · Scientific Reports · doi:10.1038/s41598-024-57898-y · Cited by 8 · see citing works
“In disease, however, the disruption of this balance, due to metabolic, hormonal, or genetic alterations generally results in deregulated bone resorption by OCs, leading to net bone loss and skeletal fragility 1,11–13 .”
Yang, Z., Liang, J., Shi, D., Tuo, C., Wu, Y., & Zhang, F. (2025) · Scientific Reports · doi:10.1038/s41598-025-13217-7 · Cited by 7
“This may be attributed to increased mechanical loading and metabolic disturbances associated with obesity, which can intensify stress at the fusion segment and promote bone loss, especially in elderly female patients 30 .”
Bone marrow adipocytes in cancer: Mechanisms, models, and therapeutic implications
Bessot, A., Gunter, J. H., McGovern, J., & Bock, N. (2025) · Biomaterials · doi:10.1016/j.biomaterials.2025.123341 · Cited by 8 · see citing works
Assessment of osteoporosis and vertebral fractures with T1- and T2-weighted MRI scans
Din, R. U., Wang, L., Cheng, X., & Yang, H.-S. (2025) · Archives of Osteoporosis · doi:10.1007/s11657-025-01509-4 · Cited by 7
“Aging and a lack of sex hormones are responsible for decreasing osteoblastogenesis while increasing adipogenesis [35].”
Ketogenic diet and β-hydroxybutyrate in osteoporosis: current progress and controversy
Luo, C., Dai, Z., He, W.-H., He, Y.-Q., Yang, P., Huang, M., Li, J., Xu, Y., & Huang, W. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1508695 · Cited by 7 · see citing works
Are Dietary Patterns Relevant for Reducing the Risk of Fractures and Sarcopenia?
Welch, A., Scott, J., Cameron, D., & Yates, M. (2025) · Current Osteoporosis Reports · doi:10.1007/s11914-024-00899-7 · Cited by 7 · see citing works
Rinne, C., Soultoukis, G., Oveisi, M., Leer, M., Schmidt-Bleek, O., Burkhardt, L.-M., Bucher, C., Moussa, E. A., Makhlouf, M., Duda, G. N., et al. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1394263 · Cited by 7 · see citing works
Oxidative stress and bone marrow adipocytes: Molecular mechanisms and possible implications
Tao, H.-Q., Ge, G.-R., Chen, K., Chen, T.-R., Li, W.-M., Yang, P., Che, Y., Wang, Y.-F., Chen, W.-L., Yu, H., et al. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2025.101038 · Cited by 6 · see citing works
“Within the hypoxic bone environment, BMAT plays an important role in storing energy, secreting adipokines, and targeting them toward adjacent bone cells [25].”
Varzideh, F., Farroni, E., Kaunsakar, U., Eiwaz, M. B., Jankauskas, S., & Santulli, G. (2025) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-024-05546-z · Cited by 6 · see citing works
Nishimura, H., Murata, Y., Mullen, M. T., Yamaura, K., Singer, J., Huard, C., Lind, D. R. G., Hambright, W. S., Bahney, C. S., Philippon, M. J., et al. (2025) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1155/term/9187855 · Cited by 6 · see citing works
“Tis is especially important in the setting of age-related bone diseases where there is a reduction in cellular osteogenic capacity, leading to decreased bone mineral density in osteopenia/osteoporosis, as well as an accumulation of fatty tissue within the bone marrow [2, 3].”
Machine Learning Empowered Osteoporosis Prediction: A Comparative Analysis
Singh, Y., Ghosh, D., Gourisaria, M., Jena, J. J., Patra, S., & Panda, A. R. (2024) · International Conference Electronic Systems, Signal Processing and Computing Technologies [ICESC-] · doi:10.1109/icesc60852.2024.10689842 · Cited by 6
“Osteoporosis can be defined as a systematic disease of bones characterized by reduced bone mass and micro-architectural degradation leading to elevated fracture risk [1].”
BackgroundAzizollahi, F., Oroojalian, F., Vatanchian, M., Zak, A., Khodabandeh, A., Moqadam, K. H., & Havakhah, S. (2026) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2025.107745 · Cited by 5
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“Generally, diabetes contributes to osteoporosis through various mechanisms, including interference with metabolic processes and the effects of reactive oxygen species and inflammatory molecules [21,22].”
Nurkolis, F., Utami, T. W., Alatas, A. I., Wicaksono, D., Kurniawan, R., Ratmandhika, S. R., Sukarno, K. T., Pahu, Y. G. P., Kim, B., Tallei, T. E., et al. (2024) · Frontiers in Aging · doi:10.3389/fragi.2024.1462569 · Cited by 5 · see citing works
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“Additionally, reactive oxygen species and oxidative stress levels increase with aging, impairing osteoblast formation and promoting adipocyte differentiation [31].”
InfluentialPan, R.-Z., & Li, Y.-K. (2024) · Journal of Orthopaedic Surgery and Research · doi:10.1186/s13018-024-04991-7 · Cited by 4 · see citing works
“The ‘fattening’ of bones, coupled with reduced bone formation, lowers trabecular bone density, leading to a higher risk of fractures [40].”
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Ramadan, A., Etrusco, A., D'Amato, A., Laganà, A. S., Chiantera, V., Zgheib, C., Shoucair, H., Alakrah, W., Yared, G., & Sleiman, Z. (2024) · MITAT. Minimally invasive therapy & allied technologies · doi:10.1080/13645706.2024.2376837 · Cited by 4 · see citing works
“…becomes absolutely necessary in the case of high-complexity surgeries [38–41] and with obese patients, since the latter, in addition to involving a whole range of health problems known to the patient [42–45], makes dissection and identification of anatomical structures extremely difficult [46,47].”
Usefulness of DXA-based bone strain index in postmenopausal women with type 2 diabetes mellitus
Bonaccorsi, G., Sciavicco, G., Rinaudo, L., Brigato, A., Fiorella, G., Carnevale, A., Ulivieri, F. M., & Messina, C. (2024) · Archives of Osteoporosis · doi:10.1007/s11657-024-01411-5 · Cited by 4
Du, A., Xu, R., Yang, Q., Lu, Y., & Luo, X. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.18141 · Cited by 4
“17 The mechanisms underlying bone fractured in T2D are diverse and unresolved.”
BackgroundLi, H., Xu, Q., Ye, Y.-L., Chang, B., Wang, R., & Li, G.-W. (2024) · BMC Public Health · doi:10.1186/s12889-023-17494-7 · Cited by 4 · see citing works
“In addition, the hypermetabolic status of bone marrow stromal cells, and an accelerated senescent bone marrow microenvironment (such as expanded bone marrow adipose tissue) in obese individuals, leads to increased bone fragility [36].”
BackgroundLu, Z., Cao, H., & Hu, X.-Y. (2023) · Journal of Environmental and Public Health · doi:10.1155/2023/7571696 · Cited by 4
RetractedGut microbiota orchestrates bone homeostasis: a multi-pathway network from intestine to skeleton
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“Obesity, hyperglycemia, and dyslipidemia are established risk factors for OP, and persons who are obese and diabetic frequently present with concomitant OP (136).”
Yu, H.-D., Chen, R., Sun, S., & Zhou, R. (2026) · European Journal of Medical Research · doi:10.1186/s40001-026-04162-w · Cited by 3 · see citing works
“First, most relevant investigations have predominantly focused on the clinical implications and pathogenic mechanisms linking BMAT to osteoporosis and skeletal fragility in ageing humans with obesity or type 2 diabetes [3, 5, 34, 98].”
Ahmad, I., Gbr, S. S. A. E., Naggar, B. M. M. A. E., Abdelwahab, M. K., Elsaghier, E. O., Mohammed, D., Mohamed, M. A., Mohamed, M. S., El-Rahim, M. M. M. A. A., & attar, S. E. (2024) · BMC Women's Health · doi:10.1186/s12905-024-03311-9 · Cited by 3 · see citing works
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The role of vascular aging, bone marrow and immune system in hypertension
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“The accumulation of fat cells within the bone marrow is a critical characteristic feature of bone marrow aging process [77].”
Yang, T.-J., Chen, T.-X., Zhang, Y., Luo, Y.-Z., & Wen, P. (2025) · Frontiers in Medicine · doi:10.3389/fmed.2025.1653037 · Cited by 2 · see citing works
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“…that obesity might protect against OP, but this is refuted by the fact that obese individuals have a significantly higher risk of fractures, likely due to systemic inflammation affecting bone metabolism and increased adipogenesis leading to reduced bone mass in obese populations [11, 20–22].”
Tang, H., Zhao, J., Yan, X., Zheng, Z.-Y., Bai, W., Tang, Z., & Liu, X. (2025) · Journal of Multidisciplinary Healthcare · doi:10.2147/jmdh.s529217 · Cited by 2 · see citing works
“11 Sheng et al, however, found no significant association between overweight and obesity (assessed by BMI) and cervical diseases in a cross-sectional sample from the 2014 Medical Expenditure Panel Study (MEPS) (n = 23,048), which is considered representative of the US population.”
Birkeland, E., Bamigbetan, W., Molven, K. D., Thorsby, P., Gulseth, H., Aas, A.-M., & Dahl, C. (2025) · Archives of Osteoporosis · doi:10.1007/s11657-025-01556-x · Cited by 2 · see citing works
Association of the Chinese visceral adiposity index with marrow adiposity in postmenopausal females
Zuo, X., Miao, Z.-Y., Xu, R., Shi, D., Chang, S.-X., Li, G.-W., & Luo, P. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1542516 · Cited by 2
“Research suggests that the expansion of visceral fat is closely linked to increased adipocyte formation within the bone marrow microenvironment (37, 38).”
Klinaku, F. T., Comi, L., Giglione, C., & Magni, P. (2024) · Journal of Endocrinological Investigation · doi:10.1007/s40618-024-02516-x · Cited by 3 · see citing works
Freitas, B. P., Cândido, L. M., Wagner, K. J. P., Lacerda, A. C. R., Mendonça, V. A., Micheli, R. D., Sartório, A., de Avelar, N. C. P., & Danielewicz, A. L. (2024) · Healthcare · doi:10.3390/healthcare12161625 · Cited by 2 · see citing works
“These factors accelerate cartilage wear, contribute to muscle mass loss, and disrupt bone metabolism, leading to reduced bone quality and increased risk of functional impairments [28].”
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Aging-related metabolic dysregulation in osteoporosis: mechanisms and therapeutic strategies
Bai, R., Huang, Z.-S., Tian, X., Liu, Y.-K., Wang, Y., Su, Y., Li, M.-J., Cheng, C., Wu, J., Zha, Y.-J., et al. (2026) · Frontiers in Aging · doi:10.3389/fragi.2026.1886673 · Cited by 1 · see citing works
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Epigenetic transcriptional regulation of skeletal aging: The emerging role of m6A methylation
Song, C., Song, G., Zhang, S., Zhao, H., Wen, Z., Chen, Y., Chen, X., Liu, B., Ni, Q., & Fan, D.-P. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2026.101088 · Cited by 1 · see citing works
“While excessive adipose tissue can exert mechanical loading on bones, potentially inducing a compensatory increase in BMD, it concurrently promotes chronic low-grade inflammation and hormonal dysregulation which exert deleterious effects on bone homeostasis [6,7].”
Gong, M., Cao, T., Feng, X.-M., Ding, J., Fan, N., He, Y., & Yan, Y.-X. (2026) · NMCD. Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2026.104704 · Cited by 1 · see citing works
The Broken Cradle: Bone Marrow Stem Cell Niche Remodelling in Diabetes
Kum, J. J. Y., Howlett, C. J., & Khan, Z. A. (2025) · Stem Cell Reviews and Reports · doi:10.1007/s12015-025-11038-9 · Cited by 1 · see citing works
“Recent work has expanded this paradigm, as bone marrow adiposity is now recognized as a shared pathogenic mechanism linking osteoporosis, diabetes, and obesity, with marrow adipocytes actively secreting pro-inflammatory cytokines and adipokines that impair bone remodeling [ 104].”
Li, L.-W., Ma, Y., He, X., Cao, M.-Y., Zheng, E., & Leng, J. (2025) · BMC Geriatrics · doi:10.1186/s12877-025-06826-4 · Cited by 1 · see citing works
“Obesity can lead to alterations in the cellular structure and molecular networks of the bone microenvironment, causing changes in the volume of trabeculae and bone cortex, while increasing the mass of bone marrow adipose tissue, which has a deleterious impact on bone mass and strength [29].”
Diabetes Burnout Among the Elderly With Type 2 Diabetes
Muntamah, U., Siyamti, D., & Sianturi, M. (2025) · Window of Health : Jurnal Kesehatan · doi:10.33096/woh.vi.2615 · Cited by 1
“25 These biomedical mechanisms, when combined with cultural expectations and gendered roles, highlight the multifactorial nature of diabetes burnout in elderly women in Indonesia.”
The association between body roundness index and lumbar marrow fat content in postmenopausal women.
Luo, P., Miao, Z.-Y., Guo, M.-Y., Qin, L., Xu, R., Lu, L., Wang, Y., & Li, G.-W. (2025) · Bone · doi:10.1016/j.bone.2025.117684 · Cited by 1 · see citing works
Polypharmacy and Bone Health in Patients with Type 2 Diabetes Mellitus: A Narrative Review
Kashmoola, I. O., Mohammad, S. H., & Alsaaty, M. (2025) · Journal of Bone Metabolism · doi:10.11005/jbm.25.975 · Cited by 1
“[22] Likewise, in patients with T2DM, CKD disturbs homeostasis of minerals resulting in bone and mineral disorders.”
Li, W., Wang, W., Zhang, M., Chen, Q., Li, F., & Li, S. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1518656 · Cited by 1
Xu, L., & Cao, Y. (2025) · Archives of Dermatological Research · doi:10.1007/s00403-025-03805-y · Cited by 1 · see citing works
Liu, X., Lou, Y., Chang, Z., Gu, C.-Y., Du, B., & Sun, G.-Q. (2025) · Clinics · doi:10.1016/j.clinsp.2025.100674 · Cited by 1
“7,27 In fact, osteoporosis and fracture risk increases along with age, independently from body weight, and, in menopause, the abrupt decrease of estrogen is the primary cause of osteoporosis.”
Opportunistic Computed Tomography
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HDL levels modulate the impact of type 2 diabetes susceptibility alleles in older adults
Sullivan, S. O. ’., Hageh, C. A., Henschel, A., Chacar, S., Abchee, A., Zalloua, P., & Nader, M. (2024) · Lipids in Health and Disease · doi:10.1186/s12944-024-02039-7 · Cited by 1 · see citing works
“Indeed several chronic diseases and ageing share pathophysiological processes under-pinned by disruption of signal pathways at the molecular and cellular level [19–21].”
BackgroundAnalysis of Shared Mechanisms and Chinese Herbal Medicines Between Osteoporosis and Type 2 Diabetes
Yang, H., Luo, F., & Xiong, Z.-Y. (2023) · Pharmacognosy Magazine · doi:10.1177/09731296231215568 · Cited by 1
“Several factors, including hyperglycemia, oxidative stress, alterations in relevant cytokines and hormone levels, and the use of antidiabetic medications, have been implicated in the development of OP in individuals with T2D (Ali et al., 2022; Mo et al., 2022).”
BackgroundResearch Progress of Irisin in Obesity and Related Metabolic Diseases
Zhang, Y.-N. (2023) · Advances in Clinical Medicine · doi:10.12677/acm.2023.13122830 · Cited by 1 · see citing works
Lai, C.-H., LI, Y.-T., Wu, T.-S., & Wu, C.-T. (2026) · Archives of Osteoporosis · doi:10.1007/s11657-026-01785-8
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“The influence of obesity on the skeleton is context dependent and not uniformly protective (Ali et al. 2022).”
Zhang, S., Wang, H., Zhao, C., Zhu, C., Li, X., Su, Z., Zou, J., Wang, C., Zhang, L., Yuan, Y., et al. (2026) · Stem Cell Research & Therapy · doi:10.1186/s13287-026-05068-4
“…observations indicate a significant positive correlation between increased bone marrow fat content, visceral fat accumulation, and decreased bone mineral density as well as bone loss, a phenotypic association that is a typical clinical feature of age-related and postmenopausal osteoporosis [32–34].”
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Impact of Clinical Factors on Bone Microarchitecture in Patients with Turner Syndrome
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“For instance, osteoporosis, the most prevalent bone remodeling disorder globally, often exhibits heightened marrow fat content [17,18].”
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“Obesity also regulates the expression of bone anabolic molecules and disrupts intracellular signaling cascades in bone tissue [12, 41].”
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“[47] A similar complex, nonlinear interaction was also indicated between age and weight in our study.”
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“35 Glycated hemoglobin (HbA1c) has long been the gold standard for glycemic control and shown to be associated with various chronic complications of DM, such as diabetic retinopathy, diabetic nephropathy, and diabetic peripheral neuropathy.”
- Authors
- Ali, D., Tencerova, M., Figeac, F., Kassem, M., & Jafari, A.
- Affiliations
- University of Southern Denmark (DK)
- University of Copenhagen (DK)
- Corresponding author
- Ali, Dalia
- Jafari, Abbas
- Venue
- Frontiers in Endocrinology
- Publisher
- Frontiers Media SA
- Published
- 2022-09-15
- Volume
- 13
- Pages
- 981487-981487
- ISSN
- 1664-2392 (ISSN-L)
- PMC
- PMC9520254
- OpenAlex
- W4295942629
- Cited by
- 122
- References
- 220
- Citations by year
- 2026: 25 · 2025: 42 · 2024: 43 · 2023: 10 · 2022: 2
- FWCI
- 5.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Endocrinology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, cc-by)
- Funders
- Olav Thon Stiftelsen
- Grantová Agentura České Republiky
- Novo Nordisk Fonden
- Topics
- 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
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- osteoporosis, bone marrow adipose tissue, bone marrow adiposity, obesity, type 2 diabetes, aging, bone fragility, bone homeostasis, bone formation, fracture risk, postmenopausal women, older men
- MeSH terms
- Aged, Aging, Bone Marrow, Diabetes Mellitus, Type 2, Female, Humans, Male, Obesity, Osteoporosis, Adiposity, Fractures, Bone
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