Changes in Vertebral Bone Marrow Fat and Bone Mass After Gastric Bypass Surgery: A Pilot Study

Overview

Journal Bone

Specialties Endocrinology
Orthopedics

Date 2015 Jan 21

PMID 25603463

Citations 31

Authors

A L Schafer

X Li

A V Schwartz

L S Tufts

A L Wheeler

C Grunfeld

L Stewart

S J Rogers

J T Carter

A M Posselt

D M Black

D M Shoback

Affiliations

Soon will be listed here.

Abstract

Bone marrow fat may serve a metabolic role distinct from other fat depots, and it may be altered by metabolic conditions including diabetes. Caloric restriction paradoxically increases marrow fat in mice, and women with anorexia nervosa have high marrow fat. The longitudinal effect of weight loss on marrow fat in humans is unknown. We hypothesized that marrow fat increases after Roux-en-Y gastric bypass (RYGB) surgery, as total body fat decreases. In a pilot study of 11 morbidly obese women (6 diabetic, 5 nondiabetic), we measured vertebral marrow fat content (percentage fat fraction) before and 6 months after RYGB using magnetic resonance spectroscopy. Total body fat mass declined in all participants (mean ± SD decline 19.1 ± 6.1 kg or 36.5% ± 10.9%, p<0.001). Areal bone mineral density (BMD) decreased by 5.2% ± 3.5% and 4.1% ± 2.6% at the femoral neck and total hip, respectively, and volumetric BMD decreased at the spine by 7.4% ± 2.8% (p<0.001 for all). Effects of RYGB on marrow fat differed by diabetes status (adjusted p=0.04). There was little mean change in marrow fat in nondiabetic women (mean +0.9%, 95% CI -10.0 to +11.7%, p=0.84). In contrast, marrow fat decreased in diabetic women (-7.5%, 95% CI -15.2 to +0.1%, p=0.05). Changes in total body fat mass and marrow fat were inversely correlated among nondiabetic (r=-0.96, p=0.01) but not diabetic (r=0.52, p=0.29) participants. In conclusion, among those without diabetes, marrow fat is maintained on average after RYGB, despite dramatic declines in overall fat mass. Among those with diabetes, RYGB may reduce marrow fat. Thus, future studies of marrow fat should take diabetes status into account. Marrow fat may have unique metabolic behavior compared with other fat depots.

Citing Articles

Function and Regulation of Bone Marrow Adipose Tissue in Health and Disease: State of the Field and Clinical Considerations.

Zhang X, Tian L, Majumdar A, Scheller E Compr Physiol. 2024; 14(3):5521-5579.

PMID: 39109972 PMC: 11725182. DOI: 10.1002/cphy.c230016.

Bone marrow adipose tissue composition and glycemic improvements after gastric bypass surgery.

Kim T, Schwartz A, Li X, Xu K, Kazakia G, Grunfeld C Bone Rep. 2022; 17:101596.

PMID: 35734226 PMC: 9207612. DOI: 10.1016/j.bonr.2022.101596.

The dynamics of human bone marrow adipose tissue in response to feeding and fasting.

Fazeli P, Bredella M, Pachon-Pena G, Zhao W, Zhang X, Faje A JCI Insight. 2021; 6(12).

PMID: 33974568 PMC: 8262500. DOI: 10.1172/jci.insight.138636.

Impact of sleeve gastrectomy on bone outcomes in adolescents vs. adults with obesity.

Bredella M, Karzar N, Singhal V, Bose A, Animashaun A, Mitchell D Bone. 2021; 149:115975.

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Zoledronic acid for prevention of bone loss in patients receiving bariatric surgery.

Liu Y, Cote M, Cheney M, Lindeman K, Rushin C, Hutter M Bone Rep. 2021; 14:100760.

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References

Chao D, Espeland M, Farmer D, Register T, Lenchik L, Applegate W . Effect of voluntary weight loss on bone mineral density in older overweight women. J Am Geriatr Soc. 2000; 48(7):753-9. DOI: 10.1111/j.1532-5415.2000.tb04749.x. View

Botolin S, McCabe L . Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology. 2006; 148(1):198-205. DOI: 10.1210/en.2006-1006. View

Shen W, Chen J, Punyanitya M, Shapses S, Heshka S, Heymsfield S . MRI-measured bone marrow adipose tissue is inversely related to DXA-measured bone mineral in Caucasian women. Osteoporos Int. 2006; 18(5):641-7. PMC: 2034514. DOI: 10.1007/s00198-006-0285-9. View

Harris T, Launer L, Eiriksdottir G, Kjartansson O, Jonsson P, Sigurdsson G . Age, Gene/Environment Susceptibility-Reykjavik Study: multidisciplinary applied phenomics. Am J Epidemiol. 2007; 165(9):1076-87. PMC: 2723948. DOI: 10.1093/aje/kwk115. View

Bolotin H . DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodelling. Bone. 2007; 41(1):138-54. DOI: 10.1016/j.bone.2007.02.022. View

Sjostrom L, Narbro K, Sjostrom C, Karason K, Larsson B, Wedel H . Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007; 357(8):741-52. DOI: 10.1056/NEJMoa066254. View

Villareal D, Shah K, Banks M, Sinacore D, 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(6):2181-7. PMC: 2435639. DOI: 10.1210/jc.2007-1473. View

Blake G, Griffith J, Yeung D, Leung P, Fogelman I . Effect of increasing vertebral marrow fat content on BMD measurement, T-Score status and fracture risk prediction by DXA. Bone. 2008; 44(3):495-501. DOI: 10.1016/j.bone.2008.11.003. View

Thaler J, Cummings D . Minireview: Hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology. 2009; 150(6):2518-25. DOI: 10.1210/en.2009-0367. View

10.

Devlin M . Why does starvation make bones fat?. Am J Hum Biol. 2011; 23(5):577-85. PMC: 3169094. DOI: 10.1002/ajhb.21202. View

11.

Naressi A, Couturier C, Castang I, de Beer R, Graveron-Demilly D . Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput Biol Med. 2001; 31(4):269-86. DOI: 10.1016/s0010-4825(01)00006-3. View

12.

Schellinger D, Lin C, Hatipoglu H, Fertikh D . Potential value of vertebral proton MR spectroscopy in determining bone weakness. AJNR Am J Neuroradiol. 2001; 22(8):1620-7. PMC: 7974571. View

13.

Bredella M, Fazeli P, Miller K, Misra M, Torriani M, Thomas B . Increased bone marrow fat in anorexia nervosa. J Clin Endocrinol Metab. 2009; 94(6):2129-36. PMC: 2690416. DOI: 10.1210/jc.2008-2532. View

14.

Khoo B, Brown K, Cann C, Zhu K, Henzell S, Low V . Comparison of QCT-derived and DXA-derived areal bone mineral density and T scores. Osteoporos Int. 2008; 20(9):1539-45. DOI: 10.1007/s00198-008-0820-y. View

15.

Devlin M, Cloutier A, Thomas N, Panus D, Lotinun S, Pinz I . Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res. 2010; 25(9):2078-88. PMC: 3127399. DOI: 10.1002/jbmr.82. View

16.

Li X, Kuo D, Schafer A, Porzig A, Link T, Black D . Quantification of vertebral bone marrow fat content using 3 Tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging. 2011; 33(4):974-9. PMC: 3072841. DOI: 10.1002/jmri.22489. View

17.

Sheu Y, Cauley J . The role of bone marrow and visceral fat on bone metabolism. Curr Osteoporos Rep. 2011; 9(2):67-75. PMC: 4188476. DOI: 10.1007/s11914-011-0051-6. View

18.

Griffith J, Yeung D, Leung J, Kwok T, Leung P . Prediction of bone loss in elderly female subjects by MR perfusion imaging and spectroscopy. Eur Radiol. 2011; 21(6):1160-9. DOI: 10.1007/s00330-010-2054-6. View

19.

Craig C, Marshall A, Sjostrom M, Bauman A, Booth M, Ainsworth B . International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003; 35(8):1381-95. DOI: 10.1249/01.MSS.0000078924.61453.FB. View

20.

Ensrud K, Ewing S, Stone K, Cauley J, Bowman P, Cummings S . Intentional and unintentional weight loss increase bone loss and hip fracture risk in older women. J Am Geriatr Soc. 2003; 51(12):1740-7. DOI: 10.1046/j.1532-5415.2003.51558.x. View