Bone structural changes after gastric bypass surgery evaluated by HR-pQCT: a two-year longitudinal study

Vikram V Shanbhogue, René Klinkby Støving, Katrine Hartmund Frederiksen, Stine Hanson, Kim Brixen, Jeppe Gram, Niklas Rye Jørgensen, Stinus Hansen, Vikram V Shanbhogue, René Klinkby Støving, Katrine Hartmund Frederiksen, Stine Hanson, Kim Brixen, Jeppe Gram, Niklas Rye Jørgensen, Stinus Hansen

Abstract

Objective, design and methods: Roux-en-Y gastric bypass (RYGB) has proved successful in attaining sustained weight loss but may lead to metabolic bone disease. To assess impact on bone mass and structure, we measured a real bone mineral density at the hip and spine by dual-energy X-ray absorptiometry, and volumetric BMD (vBMD) and bone microarchitecture at the distal radius and tibia by high-resolution peripheral quantitative CT in 25 morbidly obese subjects (15 females, 10 males) at 0, 12 and 24 months after RYGB. Bone turnover markers (BTMs), calciotropic and gut hormones and adipokines were measured at the same time points.

Results: After a 24.1% mean weight loss from baseline to month 12 (P < 0.001), body weight plateaued from month 12 to 24 (-0.9%, P = 0.50). However, cortical and trabecular vBMD and microarchitecture deteriorated through the 24 months, such that there was a 5 and 7% reduction in estimated bone strength at the radius and tibia respectively (both P < 0.001). The declines observed in the first 12 months were matched or exceeded by declines in the 12- to 24-month period. While a significant increase in BTMs and decrease in leptin and insulin were seen at 24 months, these changes were maximal at month 12 and stabilized from month 12 to 24.

Conclusions: Despite weight stabilization and maintenance of metabolic parameters, bone loss and deterioration in bone strength continued and were substantial in the second year. The clinical importance of these changes in terms of increased risk of developing osteoporosis and fragility fractures remain an important concern.

© 2017 The authors.

Figures

Figure 1
Figure 1
Flowchart of inclusion.
Figure 2
Figure 2
Percent change in HR-pQCT parameters in radius one (grey bars) and two years (black bars) after gastric bypass surgery. *P < 0.05, **P < 0.01, ***P < 0.001 vs baseline #P < 0.05, ##P < 0.01, ###P < 0.001 vs one-year value. Trabecular net. inhomo, trabecular network inhomogeneity.
Figure 3
Figure 3
Percent change in HR-pQCT parameters in tibia one (grey bars) and two years (black bars) after gastric bypass surgery. *P < 0.05, **P < 0.01, ***P < 0.001 vs baseline #P < 0.05, ##P < 0.01, ###P < 0.001 vs one-year value. Trabecular net. inhomo, trabecular network inhomogeneity.

References

    1. Sturm R, Hattori A. Morbid obesity rates continue to rise rapidly in the United States. International Journal of Obesity 2013. 37 889–891. (10.1038/ijo.2012.159)
    1. Bray GA, Fruhbeck G, Ryan DH, Wilding JP. Management of obesity. Lancet 2016. 387 1947–1956. (10.1016/S0140-6736(16)00271-3)
    1. Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA 2002. 288 2793–2796. (10.1001/jama.288.22.2793)
    1. Chang SH, Stoll CR, Song J, Varela JE, Eagon CJ, Colditz GA. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surgery 2014. 149 275–287. (10.1001/jamasurg.2013.3654)
    1. Fleischer J, Stein EM, Bessler M, Della Badia M, Restuccia N, Olivero-Rivera L, McMahon DJ, Silverberg SJ. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. Journal of Clinical Endocrinology and Metabolism 2008. 93 3735–3740. (10.1210/jc.2008-0481)
    1. Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B, Bessler M, Zhou B, Wang J, Guo XE, et al. Bariatric surgery results in cortical bone loss. Journal of Clinical Endocrinology and Metabolism 2013. 98 541–549. (10.1210/jc.2012-2394)
    1. Yu EW, Bouxsein ML, Roy AE, Baldwin C, Cange A, Neer RM, Kaplan LM, Finkelstein JS. Bone loss after bariatric surgery: discordant results between DXA and QCT bone density. Journal of Bone and Mineral Research 2014. 29 542–550. (10.1002/jbmr.2063)
    1. Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. Journal of Clinical Endocrinology and Metabolism 2004. 89 1061–1065. (10.1210/jc.2003-031756)
    1. Vilarrasa N, San Jose P, Garcia I, Gomez-Vaquero C, Miras PM, de Gordejuela AG, Masdevall C, Pujol J, Soler J, Gómez JM. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obesity Surgery 2011. 21 465–472. (10.1007/s11695-010-0338-1)
    1. Yu EW, Bouxsein ML, Putman MS, Monis EL, Roy AE, Pratt JS, Butsch WS, Finkelstein JS. Two-year changes in bone density after Roux-en-Y gastric bypass surgery. Journal of Clinical Endocrinology and Metabolism 2015. 100 1452–1459. (10.1210/jc.2014-4341)
    1. Yu EW. Bone metabolism after bariatric surgery. Journal of Bone and Mineral Research 2014. 29 1507–1518. (10.1002/jbmr.2226)
    1. Knapp KM, Welsman JR, Hopkins SJ, Fogelman I, Blake GM. Obesity increases precision errors in dual-energy X-ray absorptiometry measurements. Journal of Clinical Densitometry 2012. 15 315–319. (10.1016/j.jocd.2012.01.002)
    1. Yu EW, Thomas BJ, Brown JK, Finkelstein JS. Simulated increases in body fat and errors in bone mineral density measurements by DXA and QCT. Journal of Bone and Mineral Research 2012. 27 119–124. (10.1002/jbmr.506)
    1. Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. Journal of Clinical Endocrinology and Metabolism 2005. 90 6508–6515. (10.1210/jc.2005-1258)
    1. Frederiksen KD, Hanson S, Hansen S, Brixen K, Gram J, Jorgensen NR, Støving RK. Bone structural changes and estimated strength after gastric bypass surgery evaluated by HR-pQCT. Calcified Tissue International 2016. 98 253–262. (10.1007/s00223-015-0091-5)
    1. Andersen S, Frederiksen KD, Hansen S, Brixen K, Gram J, Stoving RK. Bone structure and estimated bone strength in obese patients evaluated by high-resolution peripheral quantitative computed tomography. Calcified Tissue International 2014. 95 19–28. (10.1007/s00223-014-9857-4)
    1. Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone 2010. 47 519–528. (10.1016/j.bone.2010.05.034)
    1. Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Ruegsegger P. Image-based micro-finite-element modeling for improved distal radius strength diagnosis: moving from bench to bedside. Journal of Clinical Densitometry 2004. 7 153–160. (10.1385/JCD:7:2:153)
    1. Hansen S, Beck Jensen JE, Rasmussen L, Hauge EM, Brixen K. Effects on bone geometry, density, and microarchitecture in the distal radius but not the tibia in women with primary hyperparathyroidism: a case-control study using HR-pQCT. Journal of Bone and Mineral Research 2010. 25 1941–1947. (10.1002/jbmr.98)
    1. Bonewald LF, Johnson ML. Osteocytes, mechanosensing and Wnt signaling. Bone 2008. 42 606–615. (10.1016/j.bone.2007.12.224)
    1. Scibora LM. Skeletal effects of bariatric surgery: examining bone loss, potential mechanisms and clinical relevance. Diabetes, Obesity nd Metabolism 2014. 16 1204–1213. (10.1111/dom.12363)
    1. Bloomberg RD, Fleishman A, Nalle JE, Herron DM, Kini S. Nutritional deficiencies following bariatric surgery: what have we learned? Obesity Surgery 2005. 15 145–154. (10.1381/0960892053268264)
    1. Hage MP, El-Hajj Fuleihan G. Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporosis International 2014. 25 423–439. (10.1007/s00198-013-2480-9)
    1. Zhao LJ, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, Deng HW. Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. Journal of Bone and Mineral Research 2008. 23 17–29. (10.1359/jbmr.070813)
    1. Pasco JA, Henry MJ, Kotowicz MA, Collier GR, Ball MJ, Ugoni AM, Nicholson GC. Serum leptin levels are associated with bone mass in nonobese women. Journal of Clinical Endocrinology and Metabolism 2001. 86 1884–1887. (10.1210/jc.86.5.1884)
    1. Blain H, Vuillemin A, Guillemin F, Durant R, Hanesse B, de Talance N, Doucet B, Jeandel C. Serum leptin level is a predictor of bone mineral density in postmenopausal women. Journal of Clinical Endocrinology and Metabolism 2002. 87 1030–1035. (10.1210/jcem.87.3.8313)
    1. Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, Cortet B. Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. Journal of Clinical Endocrinology and Metabolism 2011. 96 2703–2713. (10.1210/jc.2011-0047)
    1. Dirksen C, Jorgensen NB, Bojsen-Moller KN, Jacobsen SH, Hansen DL, Worm D, Holst JJ, Madsbad S. Mechanisms of improved glycaemic control after Roux-en-Y gastric bypass. Diabetologia 2012. 55 1890–1901. (10.1007/s00125-012-2556-7)
    1. Shanbhogue VV, Finkelstein JS, Bouxsein ML, Yu EW. Association between insulin resistance and bone structure in non-diabetic postmenopausal women. Journal of Clinical Endocrinology and Metabolism 2016. 101 3114–3122. (10.1210/jc.2016-1726)
    1. Frost HM. On the estrogen-bone relationship and postmenopausal bone loss: a new model. Journal of Bone and Mineral Research 1999. 14 1473–1477. (10.1359/jbmr.1999.14.9.1473)
    1. Guney E, Kisakol G, Ozgen G, Yilmaz C, Yilmaz R, Kabalak T. Effect of weight loss on bone metabolism: comparison of vertical banded gastroplasty and medical intervention. Obesity Surgery 2003. 13 383–388. (10.1381/096089203765887705)
    1. Hammoud A, Gibson M, Hunt SC, Adams TD, Carrell DT, Kolotkin RL, Meikle AW. Effect of Roux-en-Y gastric bypass surgery on the sex steroids and quality of life in obese men. Journal of Clinical Endocrinology and Metabolism 2009. 94 1329–1332. (10.1210/jc.2008-1598)
    1. Khosla S, Melton LJ, 3rd, Robb RA, Camp JJ, Atkinson EJ, Oberg AL, Rouleau PA, Riggs BL. Relationship of volumetric BMD and structural parameters at different skeletal sites to sex steroid levels in men. Journal of Bone and Mineral Research 2005. 20 730–740. (10.1359/JBMR.041228)
    1. Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM, Gupta CE, Peacock M, Considine RV. Serum markers of bone turnover are increased at six and 18 months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. Journal of Clinical Endocrinology and Metabolism 2010. 95 159–166. (10.1210/jc.2009-0265)
    1. Sowers MR, Zheng H, Greendale GA, Neer RM, Cauley JA, Ellis J, Johnson S, Finkelstein JS. Changes in bone resorption across the menopause transition: effects of reproductive hormones, body size, and ethnicity. Journal of Clinical Endocrinology and Metabolism 2013. 98 2854–2863. (10.1210/jc.2012-4113)
    1. Duran de Campos C, Dalcanale L, Pajecki D, Garrido AB, Jr, Halpern A.Calcium intake and metabolic bone disease after eight years of Roux-en-Y gastric bypass. Obesity Surgery 2008. 18 386–390. (10.1007/s11695-007-9393-7)
    1. Marceau P, Biron S, Lebel S, Marceau S, Hould FS, Simard S, Dumont M, Fitzpatrick LA. Does bone change after biliopancreatic diversion? Journal of Gastrointestinal Surgery 2002. 6 690–698. (10.1016/S1091-255X(01)00086-5)
    1. Lalmohamed A, de Vries F, Bazelier MT, Cooper A, van Staa TP, Cooper C, Harvey NC. Risk of fracture after bariatric surgery in the United Kingdom: population based, retrospective cohort study. BMJ 2012. 345 e5085 (10.1136/bmj.e5085)
    1. Lu CW, Chang YK, Chang HH, Kuo CS, Huang CT, Hsu CC, Huang K-C. Fracture risk after bariatric surgery: a 12-year nationwide cohort study. Medicine 2015. 94 e2087 (10.1097/MD.0000000000002087)
    1. Rousseau C, Jean S, Gamache P, Lebel S, Mac-Way F, Biertho L, Michou L, Gagnon C. Change in fracture risk and fracture pattern after bariatric surgery: nested case-control study. BMJ 2016. 354 i3794 (10.1136/bmj.i3794)

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere