Cited by 424Bariatric Surgery and OutcomesBone health and osteoporosis researchBone Metabolism and Diseases

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Gastric Bypass Surgery for Morbid Obesity Leads to an Increase in Bone Turnover and a Decrease in Bone Mass

Coates, Penelope S., Fernstrom, John D., Fernstrom, Madelyn H., Schauer, Philip R., Greenspan, Susan L.·2004·The Journal of Clinical Endocrinology & Metabolism

DOI 10.1210/jc.2003-031756

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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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BackgroundResultInfluential
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Background
Clinicians' prescribing practices for bariatric surgery patients: is there an issue?
Guedes, B. L. D. S., Montanha, M. C., Teixeira, J. J. V., Diniz, A., Silva, S. R. B., Previdelli, I. T. S., NASSER, D., Yamada, S. S., & Kimura, E. M. (2014) · Journal of Clinical Pharmacy and Therapeutics · doi:10.1111/jcpt.12217 · Cited by 7
Potential Hematology and Nutritional Complications of Bariatric Surgery
Al‐Jafar, H. (2018) · Annals of Hematology & Oncology · doi:10.26420/annhematoloncol.2018.1209 · Cited by 7
“studied bone metabolism in 25 patients at 9 months following bariatric surgery and found that bone mineral density and content were significantly diminished when the patients were compared to 30 obese control patients [79].”
Result
The effect of bariatric surgery on bone Health: From mechanism to management
Ye, Y., Yang, D., & Han, J. (2020) · Obesity Medicine · doi:10.1016/j.obmed.2020.100199 · Cited by 7
Potential Nutritional Conflicts in Bariatric and Renal Transplant Patients
Lightner, A. L., Lau, J. N., Obayashi, P. A. C., Birge, K., & Melcher, M. L. (2011) · Obesity Surgery · doi:10.1007/s11695-011-0423-0 · Cited by 7
“Since the duodenum is bypassed in a RYGBP, calcium supplementation is needed to prevent secondary hyperparathyroidism and subsequent bone loss postoperatively [15, 38, 39].”
Background
Bariatric surgery: how and why to supplement
Bordalo, L. A., Teixeira, T. F. S., Bressan, J., & Mourão, D. M. (2011) · Revista da Associação Médica Brasileira · doi:10.1016/s0104-4230(11)70025-2 · Cited by 7
Serum Bioavailable Vitamin D Concentrations and Bone Mineral Density in Women After Obesity Surgery
Botella-Carretero, J. I., Lafuente, C., Montes‐Nieto, R., Balsa, J. A., Vega‐Piñero, B., García‐Moreno, F., Peromingo, R., Galindo, J., San‐Millán, J. L., & Escobar-Morreale, H. F. (2016) · Obesity Surgery · doi:10.1007/s11695-016-2185-1 · Cited by 7
“crease in markers of bone turnover that is not related to 25hydroxyvitamin D and parathyroid hormone (PTH) concentrations [11–13].”
Background
Osteoporosis and Hepatic Steatosis: 2 Closely Related Complications in Short‐Bowel Syndrome
Parreiras‐e‐Silva, L. T., de Araújo, I. M., Elías, J., Nogueira‐Barbosa, M. H., Suen, V. M. M., Marchini, J. S., Salmón, C. E. G., & de Paula, F. J. A. (2020) · Journal of Parenteral and Enteral Nutrition · doi:10.1002/jpen.1802 · Cited by 7
Clinical factors correlated with vitamin D deficiency in patients with obesity scheduled for bariatric surgery: A single center experience
Pilone, V., Tramontano, S., Cutolo, C., Marchese, F., Pagano, A. M., Spirito, F. D., & Schiavo, L. (2020) · International Journal for Vitamin and Nutrition Research · doi:10.1024/0300-9831/a000662 · Cited by 7
Plasma Ghrelin and von Willebrand Factor Levels in Patients with Non-Traumatic Osteonecrosis of the Femoral Head
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“Expression of the ghrelin receptor, GHS-R, has been identified in both rat and human bone cells (6, 7).”
Background
Semiquantitative Assessment of Bowel Habits and Its Relation with Calcium Metabolism after Gastric Bypass Surgery: A Retrospective Study
Aarts, E. O., Berends, F. J., Janssen, I. M. C., & Schweitzer, D. H. (2010) · Journal of Obesity · doi:10.1155/2011/156164 · Cited by 6
“A study on calcium metabolism of patients who had undergone RYGB and matched controls showed that the patients needed an extra amount of 750 mg calcium per day to maintain similar PTH levels [23].”
Background
Prise en charge nutritionnelle après la chirurgie bariatrique
Folope, V., Petit, A., & Tamion, F. (2012) · Nutrition Clinique et Métabolisme · doi:10.1016/j.nupar.2012.02.001 · Cited by 6
Evaluación a largo plazo del estado nutricional, composición corporal y densidad mineral ósea en mujeres operadas de bypass gástrico: impacto del nivel socioeconómico
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“Hemoglobina (g/Dl) [12-16] 12,5 ± 2 12,3 ± 2a 13,8 ± 1 13,1 ± 0,8 0,024”
Nutritional Management after Bariatric Surgery
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Changes in Bone Mineral Parameters after Sleeve Gastrectomy Relationship with Ghrelin and Plasma Adipokin Levels
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“Another study showed that both plasma ghrelin and BMD were significantly reduced at 11 months after sleeve gastrectomy (25).”
Background
The Influence of Different Cholecalciferol Supplementation Regimes on 25(OH) Cholecalciferol, Calcium and Parathyroid Hormone after Bariatric Surgery
Smelt, H. J. M., Pouwels, S., & Smulders, J. F. (2019) · Medicina · doi:10.3390/medicina55060252 · Cited by 6
“Supplementation with 400–800 IU of vitamin D might not provide adequate protection for postoperative patients against an increase in PTH and bone resorption [13,14].”
Background
Adequate vitamin D supplementation does not ameliorate bone loss following long limb-biliopancreatic diversion in morbidly obese women
Volonakis, S., Koika, V., Tzavelas, G., Skopeliti, M., Skroubis, G., Kalfarentzos, F. E., & Alexandrides, T. K. (2020) · HORMONES · doi:10.1007/s42000-020-00254-2 · Cited by 6
Nutritional Deficiencies Following Bariatric Surgery
Goldenberg, L. (2008) · Cited by 6
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Bone loss after bariatric surgery is observed mainly in the hip trabecular compartment and after hypoabsorptive techniques
Gómez‐Vaquero, C., Picazo, M. L., Humbert, L., Hernández-Montoliu, L., Jermakova, O., Huanuco, L., Silva, M., Osorio, J., Lazzara, C., Sobrino, L., et al. (2024) · Bone · doi:10.1016/j.bone.2024.117270 · Cited by 5
Bariatric Surgery and Effects on Calcium and Bone Metabolism
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“However, leptin, which is released by adipocytes, and its level have been shown to be significantly lower in subjects following gastric bypass surgery compared to obese controls [18, 63].”
Background
Does Bariatric Surgery Increase the Formation of Parathyroid Adenoma
Keskin, M., Öztürk, D., Koca, A. O., Ertuğrul, D. T., & Buluş, H. (2020) · Bariatric Surgical Practice and Patient Care · doi:10.1089/bari.2019.0043 · Cited by 5
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“Regarding the association between BS and the development of osteoporosis, Coates et al. (2004) observed a significant increase in bone turnover one year post-surgery.”
BackgroundResult
Role of the Primary Care Physician Before and After Weight-Loss Surgery
Neff, L. M., & Saltzman, E. J. (2005) · Obesity Management · doi:10.1089/obe.2005.1.147 · Cited by 5
Bone Loss
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Nonskeletal Risk Factors for Osteoporosis and Fractures
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Bariatric surgery in an obese patient with Albright hereditary osteodystrophy: a case report
Ferrario, C., Gastaldi, G., Portmann, L., & Giusti, V. (2013) · Journal of Medical Case Reports · doi:10.1186/1752-1947-7-111 · Cited by 4
“It has been known for more than 50 years that osteomalacia and osteoporosis are frequent complications of gastric surgery and small bowel malabsorptive disorders [7].”
Background
Clinical practice guidelines for evaluation and treatment of osteoporosis associated to endocrine and nutritional conditions
Reyes‐García, R., Gimeno, E. J., Martín, A. G., Muñoz, M. R., Sáez, J. M. G., Fernández, I. L., Varsavsky, M., Iglesias, S. G., Rodríguez, I. C., Ballesteros-Pomar, M. D., et al. (2012) · Endocrinología y Nutrición (English Edition) · doi:10.1016/j.endoen.2012.01.004 · Cited by 4
Bone metabolism and fracture risk after Biliopancreatic Diversion
Ramos, M. A., Ballesteros-Pomar, M. D., Fondo, A. M. U., González-Herráez, L., de Francisco, T. G., Sierra, M., & Rodríguez, I. M. C. (2021) · Endocrinología Diabetes y Nutrición (English ed ) · doi:10.1016/j.endien.2021.06.003 · Cited by 4
Surgical Management of Obesity and Postoperative Care
Blackburn, G. L., Olbers, T., Schneider, B. E., Sanchez, V. M., Brennan, A., Mantzoros, C. S., & Jones, D. B. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-453-1_17 · Cited by 4
Lessons from rodent gastric bypass model of enteric hyperoxaluria
Kwenda, E. P., Rabley, A. K., & Canales, B. K. (2020) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0000000000000613 · Cited by 4
Trastornos nutricionales tras cirugía bariátrica y su tratamiento
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Osteoporotic Hip Fracture as a Delayed Complication of Bariatric Surgery
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“Patients are often started on supplements soon after surgery since increased bone resorption has been reported as early as three months after surgery [18].”
Background
Preserving Duodenal Passage for Bone Mineralization: Billroth I versus Billroth II Reconstruction After Partial Gastrectomy in Growing Minipigs
Königsrainer, I., Königsrainer, A., & Maier, G. W. (2008) · Journal of Surgical Research · doi:10.1016/j.jss.2008.07.026 · Cited by 4
“Recent data in morbid obesity surgery have shown that the Roux-en-Y gastric bypass results in an increase in bone resorption associated with a decrease in bone mass [8, 9].”
Ghrelin plasma levels, gastric ghrelin cell density and bone mineral density in women with rheumatoid arthritis
Maksud, F. A. N., Kakehasi, A. M., Guimarães, M. F. B. D. R., Machado, C. J., & Barbosa, A. J. A. (2017) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20175977 · Cited by 4
“(34) found a significant decrease in serum ghrelin levels and BMD in patients undergoing gastrectomy for bariatric surgery, supporting the importance of the stomach endocrine cells in BMD.”
Background
Calcium, Parathormone, and Vitamin D Abnormalities among Roux-en-Y Gastric Bypass Patients
Pradhan, K. R., Larson, C. J., Mathiason, M. A., Lambert, P. J., Riess, K. P., Baker, M. T., & Kothari, S. N. (2008) · Bariatric Nursing and Surgical Patient Care · doi:10.1089/bar.2008.9962 · Cited by 4
“2 Ybarra et al .”
A scoping review of the phenomenon of osteoporosis in post bariatric surgical patients
Mori, C., Sheehan, D. K., Graor, C. H., & Petrinec, A. B. (2020) · International Journal of Orthopaedic and Trauma Nursing · doi:10.1016/j.ijotn.2020.100835 · Cited by 3
Depo-Provera (depot medroxyprogesterone acetate) use after bariatric surgery
Murthy, A., & Lam, C. J. (2016) · Open Access Journal of Contraception · doi:10.2147/oajc.s84097 · Cited by 3
“Lower calcium levels are a direct result of poor absorption of calcium due to loss of the proximal bowel location of absorption as well as decreased dietary intake.(17) Not much data exist on bone loss following the SG procedure.”
Cortical Bone Loss Following Gastric Bypass Surgery Is Not Primarily Endocortical
Sadoughi, S., Pasco, C., Joseph, G. B., Wu, P., Schafer, A. L., & Kazakia, G. J. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4512 · Cited by 3
Effects of bariatric surgery on bone metabolism: focusing on vitamin D
Avdeeva, V. A., Suplotova, L. A., & Rozhinskaya, L. Y. (2022) · Obesity and metabolism · doi:10.14341/omet12702 · Cited by 6
Chirurgie bariatrique : que doit savoir un pharmacien?
Giroux, I. (2010) · Pharmactuel · Cited by 3

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
DOI: 10.1210/jc.2003-031756
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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Gastric Bypass Surgery for Morbid Obesity Leads to an Increase in Bone Turnover and a Decrease in Bone Mass

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