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Gastric Bypass Surgery for Morbid Obesity Leads to an Increase in Bone Turnover and a Decrease in Bone Mass
Abstract
Little is known about the effects on the skeleton of laparoscopic Roux-en-Y gastric bypass (LRGB) surgery for morbid obesity and subsequent weight loss. We compared 25 patients who had undergone LRGB 11 ± 3 months previously with 30 obese controls matched for age, gender, and menopausal status. Compared with obese controls, patients post LRGB had significantly lower weight (92 ± 16 vs. 133 ± 20 kg; P < 0.001) and body mass index (31 ± 5 vs. 48 ± 7 kg/m2; P < 0.001). Markers of bone turnover were significantly elevated in patients post LRGB compared with controls (urinary N-telopeptide cross-linked collagen type 1, 93 ± 38 vs. 24 ± 11 nmol bone collagen equivalents per mmol creatinine; and osteocalcin, 11.6 ± 3.4 vs. 7.6 ± 3.6 ng/ml; both P < 0.001). Fifteen patients were studied prospectively for an average of 9 months after LRGB. They lost 37 ± 9 kg and had a 29 ± 8% fall in body mass index (both P < 0.001). Urinary N-telopeptide cross-linked collagen type 1 increased by 174 ± 168% at 3 months (P < 0.01) and 319 ± 187% at 9 months (P < 0.01). Bone mineral density decreased significantly at the total hip (7.8 ± 4.8%; P < 0.001), trochanter (9.3 ± 5.7%; P < 0.001), and total body (1.6 ± 2.0%; P < 0.05), with significant decreases in bone mineral content at these sites. In summary, within 3 to 9 months after LRGB, morbidly obese patients have an increase in bone resorption associated with a decrease in bone mass. Additional studies are needed to examine these findings over the longer term.
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“Vitamin D deficiency is widespread9, 10”
From Bone loss after bariatric surgery: causes, consequences, and management (2014) · cites this paper as [10]
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“In case of excessive bloating, flatulence and/or foul-smelling stools, the recommended treatments are oral neomycin or metronidazole or pancreatic enzymes (EL A, B, C and D) [18, 83, 195–220].”
BackgroundASMBS Allied Health Nutritional Guidelines for the Surgical Weight Loss Patient
Aills, L., Blankenship, J. D., Buffington, C. K., Furtado, M. M., & Parrott, J. M. (2008) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2008.03.002 · Cited by 600
“Supplementation with calcium and vitamin D during all weight loss modalities is critical to preventing bone resorption [121].”
BackgroundNutritional Deficiencies following Bariatric Surgery: What Have We Learned?
Bloomberg, R. D., Fleishman, A., Nalle, J. E., Herron, D. M., & Kini, S. U. (2005) · Obesity Surgery · doi:10.1381/0960892053268264 · Cited by 514
Long-Term Impact of Bariatric Surgery on Body Weight, Comorbidities, and Nutritional Status
Shah, M., Simha, V., & Garg, A. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0557 · Cited by 425
“(80), who followed subjects for 9 and 24 months, respectively, reported elevated markers of bone turnover and/or decreased bone mass in patients who underwent RYGB surgery, compared with patients who underwent GB surgery (80) or the matched obese controls (79, 80).”
BackgroundMechanick, J. I., Kushner, R. F., Sugerman, H. J., González-Campoy, J. M., Collazo–Clavell, M. L., Guven, S., Spitz, A. F., Apovian, C. M., Livingston, E. H., Brolin, R. E., et al. (2008) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2008.08.009 · Cited by 384
“[EL 3] [572] Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan LS.”
Bone Metabolism in Obesity and Weight Loss
Shapses, S. A., & Sukumar, D. (2012) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.012809.104655 · Cited by 358
Nutrient deficiencies secondary to bariatric surgery
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Mechanick, J. I., Kushner, R. F., Sugerman, H. J., González-Campoy, J. M., Collazo–Clavell, M. L., Spitz, A. F., Apovian, C. M., Livingston, E. H., Brolin, R. E., Sarwer, D. B., et al. (2009) · Obesity · doi:10.1038/oby.2009.28 · Cited by 346
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Interdisciplinary European Guidelines on Metabolic and Bariatric Surgery
Fried, M., Yumuk, V., Oppert, J., Scopinaro, N., Torres, A. J., Weiner, R. A., Yashkov, Y. I., & Frühbeck, G. (2013) · Obesity Facts · doi:10.1159/000355480 · Cited by 325
Prevalence of nutrient deficiencies in bariatric patients
Toh, S. Y., Zarshenas, N., & Jorgensen, J. (2009) · Nutrition · doi:10.1016/j.nut.2009.03.012 · Cited by 315
“maintaining serum 25(OH)D (albeit low), iPTH, and calcium levels on 1200 mg calcium and 400 to 800 IU vitamin D supplementation [34].”
BackgroundNutritional and Metabolic Complications of Bariatric Surgery
Malinowski, S. S. (2006) · The American Journal of the Medical Sciences · doi:10.1097/00000441-200604000-00009 · Cited by 310
Bult, M. J. F., van Dalen, T., & Muller, A. F. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0145 · Cited by 310
“Three months after gastric bypass, bone resorbtion markers are already increased and 9 months post-operatively loss of bone mineral at the spine, hip, and total body has been described (102).”
Best Practice Updates for Pediatric/Adolescent Weight Loss Surgery
Pratt, J. S. A., Lenders, C. M., Dionne, E. A., Hoppin, A. G., Hsu, G. L. K., Inge, T. H., Lawlor, D. F., Marino, M. F., Meyers, A. F., Rosenblum, J., et al. (2009) · Obesity · doi:10.1038/oby.2008.577 · Cited by 304
“The majority of patients undergoing WLS will develop some nutritional deficiency; therefore, strict preoperative (for those deficient in one or more nutrients) and postoperative adherence to multivitamin and mineral supplementation is critical for preventing severe complications (29,74,75).”
Inter-disciplinary European guidelines on surgery of severe obesity
Fried, M., Hainer, V., Basdevant, A., Buchwald, H., Deitel, M., Finer, N., Greve, J.-W. M., Horber, F., Mathus-Vliegen, E. M. H., Scopinaro, N., et al. (2007) · International Journal of Obesity · doi:10.1038/sj.ijo.0803560 · Cited by 301
Simulated increases in body fat and errors in bone mineral density measurements by DXA and QCT
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Preoperative Nutritional Status of Patients Undergoing Roux-en-Y Gastric Bypass for Morbid Obesity
Flancbaum, L., Belsley, S., Drake, V., Colarusso, T., & Tayler, E. B. (2006) · Journal of Gastrointestinal Surgery · doi:10.1016/j.gassur.2006.03.004 · Cited by 293
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“Our data confirm a prior report (7) of reduced urinary calcium excretion in patients with declining bone density after gastric bypass.”
BackgroundResultFollow-up of Nutritional and Metabolic Problems After Bariatric Surgery
Fujioka, K. (2005) · Diabetes Care · doi:10.2337/diacare.28.2.481 · Cited by 260
Obesity and Bone: A Complex Relationship
Rinonapoli, G., Pace, V., Ruggiero, C., Ceccarini, P., Bisaccia, M., Meccariello, L., & Caraffa, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413662 · Cited by 280
“Another hypothesized mechanism to explain bone loss after bariatric surgery is the reduction of lean mass, which would lead to a decline in aBMD [13,189,204,205].”
BackgroundBone, Body Weight, and Weight Reduction: What Are the Concerns?
Shapses, S. A., & Riedt, C. S. (2006) · The Journal of Nutrition · doi:10.1093/jn/136.6.1453 · Cited by 247
Nutritional deficiency after gastric bypass: diagnosis, prevention and treatment
Poitou, C., Ciangura, C., Coupaye, M., Czernichow, S., Bouillot, J., & Basdevant, A. (2007) · Diabetes & Metabolism · doi:10.1016/j.diabet.2006.11.004 · Cited by 232
Fracture risk following bariatric surgery: A population-based study
Nakamura, K. M., Haglind, E. G. C., Clowes, J. A., Achenbach, S. J., Atkinson, E. J., Melton, L. J., & Kennel, K. A. (2014) · Osteoporosis International · doi:10.1007/s00198-013-2463-x · Cited by 227
“Although a trial of high-dose vitamin D supplementation in vitamin D-deficient women reported an attenuation of BMD decline following bariatric surgery [41], the impact of vitamin D on fracture risk after bariatric surgery remains uncertain.”
InfluentialBone Metabolism After Bariatric Surgery
Yu, E. W.-Y. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2226 · Cited by 218
“Numerous studies document elevated urinary and serum bone turnover markers, beginning as early as 3 months after surgery((19,34,35,42,43)) that remain elevated throughout the second postoperative year((19,36,44)) (Table 2).”
InfluentialChange in fracture risk and fracture pattern after bariatric surgery: nested case-control study
Rousseau, C., Jean, S., Gamache, P., Lebel, S., Mac‐Way, F., Biertho, L. D., Michou, L., & Gagnon, C. (2016) · BMJ · doi:10.1136/bmj.i3794 · Cited by 203
Bone loss after bariatric surgery: causes, consequences, and management
Stein, E. M., & Silverberg, S. J. (2014) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70183-9 · Cited by 199
Oh, K. W., Lee, W., Rhee, E., Baek, K. H., Yoon, K., Kang, M. I., Yun, E. J., Park, C., Ihm, S. H., Choi, M. G., et al. (2005) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2005.02312.x · Cited by 200
Mechanick, J. I., Kushner, R. F., Sugerman, H. J., González-Campoy, J. M., Collazo–Clavell, M. L., Guven, S., Spitz, A. F., Apovian, C. M., Livingston, E. H., Brolin, R. E., et al. (2008) · Endocrine Practice · doi:10.4158/ep.14.s1.1 · Cited by 194
“[EL 3] [572] Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan LS.”
Self-citationCoupaye, M., Puchaux, K., Bogard, C., Msika, S., Jouet, P., Clerici, C., Larger, E., & Ledoux, S. (2009) · Obesity Surgery · doi:10.1007/s11695-008-9571-2 · Cited by 190
“The prevalence of vitamin D deficits and parathyroid hormone stimulation have been described as either increased [30–32] or unchanged after bariatric surgery [23], as in the present study.”
BackgroundBariatric surgery for pediatric extreme obesity: now or later?
Inge, T. H., Xanthakos, S. A., & Zeller, M. H. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803525 · Cited by 188
Johnson, J. M., Maher, J. W., Samuel, I., Heitshusen, D. S., Doherty, C., & Downs, R. W. (2005) · Journal of Gastrointestinal Surgery · doi:10.1016/j.gassur.2005.07.012 · Cited by 179
“In addition, several small studies with short follow-ups have suggested that BMD decreases after gastric bypass procedures.(8,10) It is known that the majority of calcium is absorbed in the duodenum and proximal jejunum, so bypassing this portion of the intestines might naturally predispose individuals to hypocalcemia.”
Bone Health After Bariatric Surgery
Gagnon, C., & Schafer, A. L. (2018) · JBMR Plus · doi:10.1002/jbm4.10048 · Cited by 182
“Indeed, a number of studies have reported that those with greater decline in lean mass have greater decline in aBMD by DXA((35,41,51,56,61)) or deterioration in microstructure by HR-pQCT.”
BackgroundLalmohamed, A., de Vries, F., Bazelier, M. T., Cooper, A., van Staa, T.-P., Cooper, C., & Harvey, N. C. (2012) · BMJ · doi:10.1136/bmj.e5085 · Cited by 173
Interdisciplinary European Guidelines on Surgery of Severe Obesity
Fried, M., Hainer, V., Basdevant, A., Buchwald, H., Deitel, M., Finer, N., Greve, J. W. M., Horber, F., Mathus-Vliegen, E. M. H., Scopinaro, N., et al. (2008) · Obesity Facts · doi:10.1159/000113937 · Cited by 171
True fractional calcium absorption is decreased after Roux-en-Y gastric bypass surgery
Riedt, C. S., Brolin, R. E., Sherrell, R. M., Field, M. P., & Shapses, S. A. (2006) · Obesity · doi:10.1038/oby.2006.226 · Cited by 166
“25OHD levels were low in 52% of the subjects before surgery and did not change significantly after surgery, which is consistent with other studies (20,25,28,30).”
BackgroundResultInterdisciplinary European Guidelines for Surgery for Severe (Morbid) Obesity
Fried, M., Hainer, V., Basdevant, A., Buchwald, H., Deitel, M., Finer, N., Greve, J. W. M., Horber, F., Mathus-Vliegen, E. M. H., Scopinaro, N., et al. (2007) · Obesity Surgery · doi:10.1007/s11695-007-9025-2 · Cited by 166
Mechanism Underlying the Weight Loss and Complications of Roux-en-Y Gastric Bypass. Review
Abdeen, G., & le Roux, C. (2016) · Obesity Surgery · doi:10.1007/s11695-015-1945-7 · Cited by 162
“Calcium can be released from bone as evident from the increased bone turnover and subsequent reduced bone mass after RYGB [190, 191].”
BackgroundPrevalence of vitamin D depletion among morbidly obese patients seeking gastric bypass surgery
Carlin, A. M., Rao, D. S., Meslemani, A. M., Genaw, J. A., Parikh, N. J., Levy, S., Bhan, A., & Talpos, G. B. (2006) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2005.12.001 · Cited by 162
“[3] Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan”
BackgroundMetabolic Bone Disease after Gastric Bypass Surgery for Obesity
Prisco, C. D., & Levine, S. N. (2005) · The American Journal of the Medical Sciences · doi:10.1097/00000441-200502000-00001 · Cited by 161
The Bone-Adipose Axis in Obesity and Weight Loss
Gómez‐Ambrosi, J., Rodrı́guez, A., Catalán, V., & Frühbeck, G. (2008) · Obesity Surgery · doi:10.1007/s11695-008-9548-1 · Cited by 160
“Although in several studies, an increase in PTH concentrations is the mechanism suggested to explain the bone loss observed after RYGPB [105, 107, 111], this increase is not univocally observed [ 96 , 112].”
BackgroundResultInfluentialTargeting the Incretin/Glucagon System With Triagonists to Treat Diabetes
Capozzi, M. E., DiMarchi, R. D., Tschöp, M. H., Finan, B., & Campbell, J. E. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00117 · Cited by 153
Bone Loss After Bariatric Surgery: Discordant Results Between DXA and QCT Bone Density
Yu, E. W.-Y., Bouxsein, M., Roy, A. E., Baldwin, C. M., Cange, A., Neer, R. M., Kaplan, L. M., & Finkelstein, J. S. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2063 · Cited by 155
Nutritional deficiencies after bariatric surgery
Davies, D. J., Baxter, J. M., & BAXTER, J. N. (2007) · Obesity Surgery · doi:10.1007/s11695-007-9208-x · Cited by 152
Fracture Risk After Bariatric Surgery
Lu, C., Chang, Y., Chang, H., Kuo, C.-S., Huang, C.-T., Hsu, C., & Huang, K. (2015) · Medicine · doi:10.1097/md.0000000000002087 · Cited by 153
Changes in Bone Metabolism in Morbidly Obese Patients After Bariatric Surgery: A Meta-Analysis
Liu, C., Wu, D., Zhang, J., Xu, D., Xu, W., Chen, Y., Liu, B., Li, P., & Li, L. (2015) · Obesity Surgery · doi:10.1007/s11695-015-1724-5 · Cited by 156
Two-Year Changes in Bone Density After Roux-en-Y Gastric Bypass Surgery
Yu, E. W.-Y., Bouxsein, M., Putman, M. S., Monis, E. L., Roy, A. E., Pratt, J. S. A., Butsch, W. S., & Finkelstein, J. S. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-4341 · Cited by 148
Savvidis, C., Tournis, S., & Dede, A. D. (2018) · HORMONES · doi:10.1007/s42000-018-0018-4 · Cited by 155
Clinical Management After Bariatric Surgery: Value of a Multidisciplinary Approach
McMahon, M. M., Sarr, M. G., Clark, M. M., Gall, M. M., Knoetgen, J., Service, F. J., Laskowski, E. R., & Hurley, D. L. (2006) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(11)61179-8 · Cited by 144
Bariatric surgery results in cortical bone loss
Stein, E. M., Carrelli, A., Young, P., Bucovsky, M., Zhang, C., Schrope, B., Bessler, M., Zhou, B., Wang, J., Guo, X. E., et al. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2394 · Cited by 139
Calorie Intake and Meal Patterns up to 4 Years after Roux-en-Y Gastric Bypass Surgery
Wardé-Kamar, J., Rogers, M., Flancbaum, L., & Laferrère, B. (2004) · Obesity Surgery · doi:10.1381/0960892041975668 · Cited by 140
Risks and benefits of bariatric surgery: current evidence.
Brethauer, S. A., Chand, B., & Schauer, P. R. (2006) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.73.11.993 · Cited by 139
Self-citationGrethen, E., Hill, K. M., Jones, R., Cacucci, B. M., Gupta, C. E., Acton, A., Considine, R. V., & Peacock, M. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-2280 · Cited by 136
“As we and others have shown previously (30, 53), bone turnover markers are increased in obesity.”
ResultVilarrasa, N., San José, P., García, I., Gómez-Vaquero, C., Medina Miras, P., de Gordejuela, A. G. R., Masdevall, C., Pujol, J., Soler, J., & Gómez, J. M. (2011) · Obesity Surgery · doi:10.1007/s11695-010-0338-1 · Cited by 129
Bariatric surgery, bone loss, obesity and possible mechanisms
Brzozowska, M. M., Sainsbury, A., Eisman, J. A., Baldock, P. A., & Center, J. R. (2013) · Obesity Reviews · doi:10.1111/j.1467-789x.2012.01050.x · Cited by 128
“These changes have been noted as early as 3 months post surgery (45,50,51), and occurred in spite of patients taking routinely recommended calcium and vitamin D supplements (45–47,49,54,55,57).”
BackgroundInfluentialCarlin, A. M., Rao, D. S., Yager, K. M., Parikh, N. J., & Kapke, A. (2009) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2008.08.004 · Cited by 128
Bruno, C., Fulford, A. D., Potts, J. R., McClintock, R., Jones, R., Cacucci, B. M., Gupta, C. E., Peacock, M., & Considine, R. V. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0265 · Cited by 121
“In recent reports significant decreases from presurgery measures in spine (10, 11), femoral neck (12, 13), and hip (10–13) bone mineral density have been detected, on average, 1 yr after surgery.”
BackgroundKendler, D. L., Borges, J. L. C., Fielding, R. A., Itabashi, A., Krueger, D., Mulligan, K., Camargos, B. M., Sabowitz, B., Wu, C.-H., Yu, E. W., et al. (2013) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2013.08.020 · Cited by 121
Comparison of the Absorption of Calcium Carbonate and Calcium Citrate after Roux-en-Y Gastric Bypass
Tondapu, P., Provost, D. A., ADAMS-HUET, B. A., Sims, T. L., Chang, C., & Sakhaee, K. (2009) · Obesity Surgery · doi:10.1007/s11695-009-9850-6 · Cited by 122
Anemia After Bariatric Surgery: More Than Just Iron Deficiency
von Drygalski, A., & Andris, D. A. (2009) · Nutrition in Clinical Practice · doi:10.1177/0884533609332174 · Cited by 123
Evers, S. S., Sandoval, D. A., & Seeley, R. J. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034423 · Cited by 120
Surgical Treatment of Morbid Obesity
Crookes, P. F. (2006) · Annual Review of Medicine · doi:10.1146/annurev.med.56.062904.144928 · Cited by 116
Nobili, V., Vajro, P., Dezsőfi, A., Fischler, B., Hadžić, N., Jahnel, J., Lamireau, T., McKiernan, P. J., McLin, V. A., Socha, P., et al. (2015) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000715 · Cited by 115
Vitamin D and the Bariatric Surgical Patient: A Review
Compher, C. W., Badellino, K. O., & Boullata, J. I. (2008) · Obesity Surgery · doi:10.1007/s11695-007-9289-6 · Cited by 113
“In 14 reports [20–34] representing data from 1,566 patients, only a single study [23] of 30 patients reported a mean 25-hydroxy vitamin D>80 nmol/l.”
BackgroundWeight, Dietary and Physical Activity Behaviors Two Years after Gastric Bypass
Silver, H. J., Torquati, A., Jensen, G. L., & Richards, W. O. (2006) · Obesity Surgery · doi:10.1381/096089206777822296 · Cited by 113
Wei, J.-H., Lee, W., Chong, K., Lee, Y.-C., Chen, S.-C., Huang, P., & Lin, S. (2017) · Obesity Surgery · doi:10.1007/s11695-017-2932-y · Cited by 117
Ledoux, S., Msika, S., Moussa, F., Larger, É., Boudou, P., Salomon, L., Roy, C., & Clérici, C. (2006) · Obesity Surgery · doi:10.1381/096089206778026415 · Cited by 106
Fernando Carrasco, N., Basfi-fer, K., Rojas, P., Valencia, A., Csendes, A., Codoceo, J., Inostroza, J., & Manuel Ruz, O. (2014) · Obesity Surgery · doi:10.1007/s11695-014-1179-0 · Cited by 106
“These findings are consistent with some reports in the literature showing a lack of association of bone mass loss with calcium/vitamin D supplementation and PTH concentration [19, 42, 43].”
ResultLindeman, K. G., Greenblatt, L. B., Rourke, C., Bouxsein, M., Finkelstein, J. S., & Yu, E. W.-Y. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01496 · Cited by 102
Agha‐Mohammadi, S., & Hurwitz, D. J. (2008) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e31817d6023 · Cited by 102
Metabolic Complications of Bariatric Surgery: Diagnosis and Management Issues
Mason, M. E., Jalagani, H., & Vinik, A. I. (2005) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2004.12.008 · Cited by 102
“After RYGBP, studies reveal vitamin D deficiency and decreased bone mass even when patients are advised to take 1200 mg of calcium and 400 to 800 IU of vitamin D daily [40].”
BackgroundScibora, L. M., Ikramuddin, S., Buchwald, H., & Petit, M. A. (2012) · Obesity Surgery · doi:10.1007/s11695-012-0596-1 · Cited by 101
“Prospective Changes at Hip Sites Studies exploring bone change after bariatric restrictive and malabsorptive procedures suggest that bone loss appears to preferentially affect the hip region [43, 44], including the trochanter [26, 45, 46] and femoral neck [31, 47–49].”
BackgroundResultInfluentialSchafer, A. L., Kazakia, G. J., Vittinghoff, E., Stewart, L., Rogers, S. J., Kim, T. Y., Carter, J. T., Posselt, A. M., Pasco, C., Shoback, D., et al. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3371 · Cited by 101
Contraceptive use among women with a history of bariatric surgery: a systematic review
Paulen, M. E., Zapata, L. B., Cansino, C. D., Curtis, K. M., & Jamieson, D. J. (2010) · Contraception · doi:10.1016/j.contraception.2010.02.008 · Cited by 99
“Another study raises concerns regarding bone loss and potential fracture risk with the use of DMPA in a population already losing bone mass as a side effect of significant weight loss and nutritional deficiencies [45].”
BackgroundNutritional consequences of bariatric surgery
Xanthakos, S. A., & Inge, T. H. (2006) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/01.mco.0000232913.07355.cf · Cited by 99
Vilarrasa, N., Gómez, J. M., Elio, I., Gómez-Vaquero, C., Masdevall, C., Pujol, J., Virgili, N., Burgos, R., Sánchez-Santos, R., de Gordejuela, A. G. R., et al. (2009) · Obesity Surgery · doi:10.1007/s11695-009-9843-5 · Cited by 91
Approach to the patient with secondary osteoporosis
Hofbauer, L. C., Hamann, C., & Ebeling, P. R. (2010) · European Journal of Endocrinology · doi:10.1530/eje-10-0015 · Cited by 95
Osteoporosis in Children and Adolescents
Baroncelli, G. I., Bertelloni, S., Sodini, F., & Saggese, G. (2005) · Pediatric Drugs · doi:10.2165/00148581-200507050-00003 · Cited by 93
“[165,167-170] The degree and the duration of the deficiencies individuals who had received calcium supplementation than placedetermine the severity of bone damage.”
BackgroundBenchmarking Best Practices in Weight Loss Surgery
Lim, R. B., Blackburn, G. L., & Jones, D. B. (2010) · Current Problems in Surgery · doi:10.1067/j.cpsurg.2009.11.003 · Cited by 91
Campanha-Versiani, L., Pereira, D. A. G., Ribeiro-Samora, G. A., Ramos, A. V., Diniz, M. F. H. D. S., Marco, L. A. D., & Soares, M. M. S. (2017) · Obesity Surgery · doi:10.1007/s11695-017-2618-5 · Cited by 100
Shanbhogue, V. V., Støving, R. K., Frederiksen, K. H., Hanson, S., Brixen, K., Gram, J., Jørgensen, N. R., & Hansen, S. G. (2017) · European Journal of Endocrinology · doi:10.1530/eje-17-0014 · Cited by 93
Impact of bariatric surgery on oral health conditions: 6-months cohort study
de Moura‐Grec, P. G., Yamashita, J. M., Marsicano, J. A., Ceneviva, R., Leite, C. V. D. S., Brito, G. B., Brienze, S. L. A., & Peres, S. H. D. C. S. (2014) · International Dental Journal · doi:10.1111/idj.12090 · Cited by 92
Giusti, V, Gasteyger, C., Suter, M., Heraief, E., Gaillard, R. C., & Burckhardt, P. (2005) · International Journal of Obesity · doi:10.1038/sj.ijo.0803040 · Cited by 91
Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass
Hage, M. P., & Fuleihan, G. E. (2013) · Osteoporosis International · doi:10.1007/s00198-013-2480-9 · Cited by 93
“These increments vary widely between studies, ranging between 29 and 319 %, and have been observed as early as 3 months after surgery [76] and persisted at 18 months post-surgery [78], regardless of calcium and vitamin D supplementation.”
Vitamin D in Adipose Tissue and Serum 25‐Hydroxyvitamin D After Roux‐en‐Y Gastric Bypass
Pramyothin, P., Biancuzzo, R. M., Lu, Z., Hess, D. T., Apovian, C. M., & Holick, M. F. (2011) · Obesity · doi:10.1038/oby.2011.170 · Cited by 88
“Reports of 25(OH)D levels after bariatric procedures have been discrepant, as studies have found either decreased (11,12), unchanged (13,14), or increased (15,16) 25(OH)D levels.”
BackgroundVilarrasa, N., de Gordejuela, A. G. R., Gómez‐Vaquero, C., Pujol, J., Elío, I., José, P. S., Toro, S., Casajoana, A., & Gómez, J. M. (2013) · Obesity Surgery · doi:10.1007/s11695-013-1016-x · Cited by 88
Valderas, J. P., Velasco, S., Solari, S., Yéssica Liberona, Z., Paola Viviani, G., Alberto Maiz, G., Escalona, A., & González, G., V (2009) · Obesity Surgery · doi:10.1007/s11695-009-9890-y · Cited by 90
“found a three-time increase in bone resorption, associated with an 8% decrease in hip BMD, in ten morbidly obese patients within 3 to 9 months after RYGB [14].”
BackgroundBariatric surgery and bone disease: from clinical perspective to molecular insights
Folli, F. B., Sabowitz, B., Schwesinger, W. H., Fanti, P., Guardado‐Mendoza, R., & Muscogiuri, G. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.115 · Cited by 89
Saltzman, E. J., Anderson, W., Apovian, C. M., Boulton, H. R. W., Chamberlain, A., Cullum‐Dugan, D., Cummings, S., Hatchigian, E., Hodges, B., Keroack, C. R., et al. (2005) · Obesity Research · doi:10.1038/oby.2005.32 · Cited by 87
Nutrition management of the post-bariatric surgery patient.
Handzlik-Orlik, G., Holecki, M., Orlik, B., Wylezol, M., & Duława, J. (2015) · Nutrition in clinical practice · doi:10.1177/0884533614564995 · Cited by 69
Mahdy, T., Attia, S. M., Farid, M., & Adulatif, A. (2008) · Obesity Surgery · doi:10.1007/s11695-008-9653-1 · Cited by 86
Sinha, N., Shieh, A., Stein, E. M., Strain, G. W., Schulman, A., Pomp, A., Gagner, M., Dakin, G. F., Christos, P. J., & Bockman, R. S. (2011) · Obesity · doi:10.1038/oby.2011.133 · Cited by 84
“However, prior studies examining sites with greater bone turnover such as hip and spine have reported lower BMD (8,11,12,18).”
BackgroundResultDixon, J. B., Strauss, B. J., Laurie, C., & O’Brien, P. E. (2007) · Obesity · doi:10.1038/oby.2007.639 · Cited by 83
Murai, I. H., Roschel, H., Dantas, W. S., Gil, S. D. S., Merege-Filho, C. A. A., de Cleva, R., de Sá‐Pinto, A. L., Lima, F., Santo, M. A., Benatti, F. B., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-00074 · Cited by 88
Risk of secondary hyperparathyroidism after laparoscopic gastric bypass surgery in obese women
Youssef, Y., Richards, W. O., Sekhar, N., Kaiser, J., Spagnoli, A., Abumrad, N., & Torquati, A. (2007) · Surgical Endoscopy · doi:10.1007/s00464-007-9228-6 · Cited by 82
“With more dramatic weight loss there is an increased risk of low bone mass and metabolic bone disease [1, 4, 6]. Coates et al. described the development of marked bone resorption and loss of bone mass in patients who undergo gastric bypass for morbid obesity [ 4 ].”
BackgroundVitamin D Insufficiency/Deficiency in Gastrointestinal Disorders
Bikle, D. D. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.07s208 · Cited by 81
“In contrast, in a smaller study of patients treated with the Roux-en-Y procedure, increased markers of bone turnover and reduced BMD were observed, but no changes in 25(OH)D or PTH were seen either in a 9-mo prospective trial or in comparison with obese controls who did not undergo the operation [25(OH)D levels were l…”
ResultNogués, X., Goday, A., Peña, M. J., Benaiges, D., de Ramón, M., Crous, X., Vial, M., Pera, M., Grande, L., Díez-Pérez, A., et al. (2010) · Cirugía Española · doi:10.1016/j.ciresp.2010.04.008 · Cited by 79
Bone mass loss after sleeve gastrectomy: A prospective comparative study with gastric bypass
Nogués, X., Goday, A., Peña, M. J., Benaiges, D., Ramón, M., Crous, X., Vial, M., Pera, M., Grande, L., Díez‐Pérez, A., et al. (2010) · Cirugía Española (English Edition) · doi:10.1016/s2173-5077(10)70015-6 · Cited by 80
Vitamin D alteration associated with obesity and bariatric surgery
Lespessailles, É., & Toumi, H. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370216688567 · Cited by 80
Metadata
- Authors
- Coates, P. S., Fernstrom, J. D., Fernstrom, M. H., Schauer, P. R., & Greenspan, S. L.
- Affiliations
- University of Pittsburgh (US)
- ORCID
- Schauer, Philip R.
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2004-03-01
- Volume
- 89
- Issue
- 3
- Pages
- 1061-1065
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2116196260
- Cited by
- 423
- References
- 34
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 6 · 2023: 1 · 2022: 10 · 2021: 14 · 2020: 25 · 2019: 9 · 2018: 16 · 2017: 23 · 2016: 21 · 2015: 20 · 2014: 33 · 2013: 23 · 2012: 20
- FWCI
- 29.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (M01RR000056, M01-RR00056-39)
- Topics
- Health Sciences › Medicine › Surgery › Bariatric Surgery and Outcomes
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Keywords
- laparoscopic Roux-en-Y gastric bypass, morbid obesity, bone turnover, bone mineral density, bone mineral content, bone resorption, osteocalcin, N-telopeptide, weight loss, bariatric surgery
- MeSH terms
- Adult, Bone and Bones, Calcium, Dietary, Female, Humans, Longitudinal Studies, Male, Middle Aged, Obesity, Morbid, Prospective Studies, Vitamin D, Gastric Bypass, Weight Loss, Bone Density, Bone Remodeling
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