Long-term trajectories of bone metabolism parameters and bone mineral density (BMD) in obese patients treated with metabolic surgery: a real-world, retrospective study.
Bariatric surgery
Bone metabolism
Serum calcium
Serum phosphate
Weight loss
Journal
Journal of endocrinological investigation
ISSN: 1720-8386
Titre abrégé: J Endocrinol Invest
Pays: Italy
ID NLM: 7806594
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
13
12
2022
accepted:
09
03
2023
medline:
25
9
2023
pubmed:
28
3
2023
entrez:
27
3
2023
Statut:
ppublish
Résumé
Potential negative effects of metabolic surgery on skeletal integrity remain a concern, since long-term data of different surgical approaches are poor. This study aimed to describe changes in bone metabolism in subjects with obesity undergoing both Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG). A single center, retrospective, observational clinical study on real-world data was performed enrolling subjects undergoing metabolic surgery. 123 subjects were enrolled (males 31: females 92; ages 48.2 ± 7.9 years). All patients were evaluated until 16.9 ± 8.1 months after surgery, while a small group was evaluated up to 4.5 years. All patients were treated after surgery with calcium and vitamin D integration. Both calcium and phosphate serum levels significantly increased after metabolic surgery and remained stable during follow-up. These trends did not differ between RYGB and SG (p = 0.245). Ca/P ratio decreased after surgery compared to baseline (p < 0.001) and this decrease remained among follow-up visits. While 24-h urinary calcium remained stable across all visits, 24-h urinary phosphate showed lower levels after surgery (p = 0.014), also according to surgery technique. Parathyroid hormone decreased (p < 0.001) and both vitamin D (p < 0.001) and C-terminal telopeptide of type I collagen (p = 0.001) increased after surgery. We demonstrated that calcium and phosphorous metabolism shows slight modification even after several years since metabolic surgery, irrespective of calcium and vitamin D supplementation. This different set point is characterized by a phosphate serum levels increase, together with a persistent bone loss, suggesting that supplementation alone may not ensure the maintenance of bone health in these patients.
Identifiants
pubmed: 36971952
doi: 10.1007/s40618-023-02066-8
pii: 10.1007/s40618-023-02066-8
doi:
Substances chimiques
Calcium
SY7Q814VUP
Vitamin D
1406-16-2
Phosphates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2133-2146Informations de copyright
© 2023. The Author(s), under exclusive licence to Italian Society of Endocrinology (SIE).
Références
Phillips BT, Shikora SA (2018) The history of metabolic and bariatric surgery: development of standards for patient safety and efficacy. Metab Clin Exp 79:97–107. https://doi.org/10.1016/j.metabol.2017.12.010
doi: 10.1016/j.metabol.2017.12.010
pubmed: 29307519
Arterburn DE, Telem DA, Kushner RF, Courcoulas AP (2020) Benefits and risks of bariatric surgery in adults: a review. JAMA 324:879–887. https://doi.org/10.1001/jama.2020.12567
doi: 10.1001/jama.2020.12567
pubmed: 32870301
Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K (2004) Bariatric surgery: a systematic review and meta-analysis. JAMA 292:1724–1737. https://doi.org/10.1001/jama.292.14.1724
doi: 10.1001/jama.292.14.1724
pubmed: 15479938
Rubino F (2013) From bariatric to metabolic surgery: definition of a new discipline and implications for clinical practice. Curr Atheroscler Rep 15:369. https://doi.org/10.1007/s11883-013-0369-x
doi: 10.1007/s11883-013-0369-x
pubmed: 24194467
Colquitt JL, Pickett K, Loveman E, Frampton GK (2014) Surgery for weight loss in adults. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD003641.pub4
doi: 10.1002/14651858.CD003641.pub4
pubmed: 25105982
pmcid: 9028049
Melissas J, Stavroulakis K, Tzikoulis V, Peristeri A, Papadakis JA, Pazouki A, Khalaj A, Kabir A (2017) Sleeve gastrectomy vs Roux-en-Y gastric bypass. Data from IFSO-European chapter center of excellence program. Obes Surg 27:847–855. https://doi.org/10.1007/s11695-016-2395-6
doi: 10.1007/s11695-016-2395-6
pubmed: 27761724
Peterli R, Wölnerhanssen BK, Peters T, Vetter D, Kröll D, Borbély Y, Schultes B, Beglinger C, Drewe J, Schiesser M et al (2018) Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss in patients with morbid obesity: the SM-BOSS randomized clinical trial. JAMA 319:255–265. https://doi.org/10.1001/jama.2017.20897
doi: 10.1001/jama.2017.20897
pubmed: 29340679
pmcid: 5833546
Grönroos S, Helmiö M, Juuti A, Tiusanen R, Hurme S, Löyttyniemi E, Ovaska J, Leivonen M, Peromaa-Haavisto P, Mäklin S et al (2020) Effect of laparoscopic sleeve gastrectomy vs Roux-en-Y gastric bypass on weight loss and quality of life at 7 years in patients with morbid obesity: the SLEEVEPASS randomized clinical trial. JAMA Surg. https://doi.org/10.1001/jamasurg.2020.5666
doi: 10.1001/jamasurg.2020.5666
pubmed: 32074268
pmcid: 7726698
Casimiro I, Sam S, Brady MJ (2019) Endocrine implications of bariatric surgery: a review on the intersection between incretins, bone, and sex hormones. Physiol Rep 7:e14111. https://doi.org/10.14814/phy2.14111
doi: 10.14814/phy2.14111
pubmed: 31134746
pmcid: 6536581
Saad RK, Ghezzawi M, Habli D, Alami RS, Chakhtoura M (2022) Fracture risk following bariatric surgery: a systematic review and meta-analysis. Osteoporos Int 33:511–526. https://doi.org/10.1007/s00198-021-06206-9
doi: 10.1007/s00198-021-06206-9
pubmed: 34988627
Thorell A, MacCormick AD, Awad S, Reynolds N, Roulin D, Demartines N, Vignaud M, Alvarez A, Singh PM, Lobo DN (2016) Guidelines for perioperative care in bariatric surgery: enhanced recovery after surgery (ERAS) society recommendations. World J Surg 40:2065–2083. https://doi.org/10.1007/s00268-016-3492-3
doi: 10.1007/s00268-016-3492-3
pubmed: 26943657
Mechanick JI, Apovian C, Brethauer S, Garvey WT, Joffe AM, Kim J, Kushner RF, Lindquist R, Pessah-Pollack R, Seger J et al (2019) Clinical practice guidelines for the perioperative nutrition, metabolic, and nonsurgical support of patients undergoing bariatric procedures - 2019 update: cosponsored by American association of clinical endocrinologists/American college of endocrinology, the obesity society, American society for metabolic & bariatric surgery, obesity medicine association, and American society of anesthesiologists. Endocr Pract 25:1346–1359. https://doi.org/10.4158/GL-2019-0406
doi: 10.4158/GL-2019-0406
pubmed: 31682518
O’Kane M, Parretti HM, Pinkney J, Welbourn R, Hughes CA, Mok J, Walker N, Thomas D, Devin J, Coulman KD et al (2020) British Obesity and Metabolic Surgery Society Guidelines on perioperative and postoperative biochemical monitoring and micronutrient replacement for patients undergoing bariatric surgery-2020 update. Obes Rev 21:e13087. https://doi.org/10.1111/obr.13087
doi: 10.1111/obr.13087
pubmed: 32743907
pmcid: 7583474
Di Lorenzo N, Antoniou SA, Batterham RL, Busetto L, Godoroja D, Iossa A, Carrano FM, Agresta F, Alarçon I, Azran C et al (2020) Clinical practice guidelines of the European Association for Endoscopic Surgery (EAES) on bariatric surgery: update 2020 endorsed by IFSO-EC, EASO and ESPCOP. Surg Endosc 34:2332–2358. https://doi.org/10.1007/s00464-020-07555-y
doi: 10.1007/s00464-020-07555-y
pubmed: 32328827
pmcid: 7214495
Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, Fried M, Hjelmesæth J, Kinzl J, Leitner DR, Makaronidis JM et al (2017) Practical recommendations of the obesity management task force of the European association for the study of obesity for the post-bariatric surgery medical management. Obes Facts 10:597–632. https://doi.org/10.1159/000481825
doi: 10.1159/000481825
pubmed: 29207379
pmcid: 5836195
Pereira FA, de Castro JA, dos Santos JE, Foss MC, Paula FJ (2007) Impact of marked weight loss induced by bariatric surgery on bone mineral density and remodeling. Braz J Med Biol Res 40:509–517. https://doi.org/10.1590/s0100-879x2007000400009
doi: 10.1590/s0100-879x2007000400009
pubmed: 17401494
Costa TL, Paganotto M, Radominski RB, Kulak CM, Borba VC (2015) Calcium metabolism, vitamin D and bone mineral density after bariatric surgery. Osteoporos Int 26:757–764. https://doi.org/10.1007/s00198-014-2962-4
doi: 10.1007/s00198-014-2962-4
pubmed: 25388022
Alencar MAVS, Araújo IM, Parreiras-E-Silva LT, Nogueira-Barbosa MH, Salgado W, Elias J, Salmon CEG, Paula FJA (2021) Hashtag bone: detrimental effects on bone contrast with metabolic benefits one and five years after Roux-en-Y gastric bypass. Braz J Med Biol Res 54:e11499. https://doi.org/10.1590/1414-431X2021e11499
doi: 10.1590/1414-431X2021e11499
pubmed: 34878062
pmcid: 8647898
Fleischer J, Stein EM, Bessler M, Della Badia M, Restuccia N, Olivero-Rivera L, McMahon DJ, Silverberg SJ (2008) The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab 93:3735–3740. https://doi.org/10.1210/jc.2008-0481
doi: 10.1210/jc.2008-0481
pubmed: 18647809
pmcid: 2579647
Riedt CS, Brolin RE, Sherrell RM, Field MP, Shapses SA (2006) True fractional calcium absorption is decreased after Roux-en-Y gastric bypass surgery. Obesity (Silver Spring) 14:1940–1948. https://doi.org/10.1038/oby.2006.226
doi: 10.1038/oby.2006.226
pubmed: 17135609
Tian Z, Fan XT, Li SZ, Zhai T, Dong J (2020) Changes in bone metabolism after sleeve gastrectomy versus gastric bypass: a meta-analysis. Obes Surg 30:77–86. https://doi.org/10.1007/s11695-019-04119-5
doi: 10.1007/s11695-019-04119-5
pubmed: 31414297
Ou X, Chen M, Xu L, Lin W, Huang H, Chen G, Wen J (2022) Changes in bone mineral density after bariatric surgery in patients of different ages or patients with different postoperative periods: a systematic review and meta-analysis. Eur J Med Res 27:144. https://doi.org/10.1186/s40001-022-00774-0
doi: 10.1186/s40001-022-00774-0
pubmed: 35934692
pmcid: 9358806
Brethauer SA, Kim J, el Chaar M, Papasavas P, Eisenberg D, Rogers A, Ballem N, Kligman M, Kothari S, ACI Committee (2015) Standardized outcomes reporting in metabolic and bariatric surgery. Surg Obes Relat Dis 11:489–506. https://doi.org/10.1016/j.soard.2015.02.003
doi: 10.1016/j.soard.2015.02.003
pubmed: 26093765
Pedrazzoni M, Girasole G, Bertoldo F, Bianchi G, Cepollaro C, Del Puente A, Giannini S, Gonnelli S, Maggio D, Marcocci C et al (2003) Definition of a population-specific DXA reference standard in Italian women: the Densitometric Italian Normative Study (DINS). Osteoporos Int 14:978–982. https://doi.org/10.1007/s00198-003-1521-1
doi: 10.1007/s00198-003-1521-1
pubmed: 14530829
Carlin AM, Zeni TM, English WJ, Hawasli AA, Genaw JA, Krause KR, Schram JL, Kole KL, Finks JF, Birkmeyer JD et al (2013) The comparative effectiveness of sleeve gastrectomy, gastric bypass, and adjustable gastric banding procedures for the treatment of morbid obesity. Ann Surg 257:791–797. https://doi.org/10.1097/SLA.0b013e3182879ded
doi: 10.1097/SLA.0b013e3182879ded
pubmed: 23470577
Angrisani L, Santonicola A, Iovino P, Vitiello A, Zundel N, Buchwald H, Scopinaro N (2017) Bariatric surgery and endoluminal procedures: IFSO Worldwide Survey 2014. Obes Surg 27:2279–2289. https://doi.org/10.1007/s11695-017-2666-x
doi: 10.1007/s11695-017-2666-x
pubmed: 28405878
pmcid: 5562777
Madeo B, De Vincentis S, Kara E, Vescini F, Trenti T, Guaraldi G, Rochira V (2019) Reliability of calcium-phosphorus (Ca/P) ratio as a new, accurate and inexpensive tool in the diagnosis of some Ca-P disorders. J Endocrinol Invest 42:1041–1049. https://doi.org/10.1007/s40618-019-01025-6
doi: 10.1007/s40618-019-01025-6
pubmed: 30796757
Greco C, Passerini F, Coluccia S, Bondi M, Mecheri F, Trapani V, Volpe A, Toschi P, Carubbi F, Simoni M et al (2022) Effects of bariatric and metabolic surgical procedures on dyslipidemia: a retrospective, observational analysis. Metab Target Organ Dam. https://doi.org/10.20517/mtod.2022.22
doi: 10.20517/mtod.2022.22
Madeo B, De Vincentis S, Repaci A, Altieri P, Vicennati V, Kara E, Vescini F, Amadori P, Balestrieri A, Pagotto U et al (2020) The calcium-to-phosphorous (Ca/P) ratio in the diagnosis of primary hyperparathyroidism and hypoparathyroidism: a multicentric study. Endocrine 68:679–687. https://doi.org/10.1007/s12020-020-02276-7
doi: 10.1007/s12020-020-02276-7
pubmed: 32236819
Wu KC, Cao S, Weaver CM, King NJ, Patel S, Kim TY, Black DM, Kingman H, Shafer MM, Rogers SJ et al (2022) Intestinal calcium absorption decreases after laparoscopic sleeve gastrectomy despite optimization of vitamin D status. J Clin Endocrinol Metab. https://doi.org/10.1210/clinem/dgac579
doi: 10.1210/clinem/dgac579
pubmed: 36190980
pmcid: 10188309
Billington EO, Murphy R, Gamble GD, Callon K, Davies N, Plank LD, Booth M, Reid IR (2019) Fibroblast growth factor 23 levels decline following sleeve gastrectomy. Clin Endocrinol (Oxf) 91:87–93. https://doi.org/10.1111/cen.13981
doi: 10.1111/cen.13981
pubmed: 30943313
Peacock M (2010) Calcium metabolism in health and disease. Clin J Am Soc Nephrol 5(Suppl 1):S23-30. https://doi.org/10.2215/CJN.05910809
doi: 10.2215/CJN.05910809
pubmed: 20089499
Schafer AL (2017) Vitamin D and intestinal calcium transport after bariatric surgery. J Steroid Biochem Mol Biol 173:202–210. https://doi.org/10.1016/j.jsbmb.2016.12.012
doi: 10.1016/j.jsbmb.2016.12.012
pubmed: 28027914
Wongdee K, Chanpaisaeng K, Teerapornpuntakit J, Charoenphandhu N (2021) Intestinal calcium absorption. Compr Physiol 11:2047–2073. https://doi.org/10.1002/cphy.c200014
doi: 10.1002/cphy.c200014
pubmed: 34058017
Wasserman RH (2004) Vitamin D and the dual processes of intestinal calcium absorption. J Nutr 134:3137–3139. https://doi.org/10.1093/jn/134.11.3137
doi: 10.1093/jn/134.11.3137
pubmed: 15514288
García Martín A, Varsavsky M, Cortés Berdonces M, Ávila Rubio V, Alhambra Expósito MR, Novo Rodríguez C, Rozas Moreno P, Romero Muñoz M, Jódar Gimeno E, Rodríguez Ortega P et al (2020) Phosphate disorders and clinical management of hypophosphatemia and hyperphosphatemia. Endocrinol Diabetes Nutr (Engl Ed) 67:205–215. https://doi.org/10.1016/j.endinu.2019.06.004
doi: 10.1016/j.endinu.2019.06.004
pubmed: 31501071
Liu C, Wu D, Zhang JF, Xu D, Xu WF, Chen Y, Liu BY, Li P, Li L (2016) Changes in bone metabolism in morbidly obese patients after bariatric surgery: a meta-analysis. Obes Surg 26:91–97. https://doi.org/10.1007/s11695-015-1724-5
doi: 10.1007/s11695-015-1724-5
pubmed: 25982806
Barzin M, Ebadinejad A, Vahidi F, Khalaj A, Mahdavi M, Valizadeh M, Hosseinpanah F (2022) The mediating role of bariatric surgery in the metabolic relationship between parathyroid hormone and 25-hydroxyvitamin D. Osteoporos Int 33:2585–2594. https://doi.org/10.1007/s00198-022-06533-5
doi: 10.1007/s00198-022-06533-5
pubmed: 35982319
Ko BJ, Myung SK, Cho KH, Park YG, Kim SG, Kim DH, Kim SM (2016) Relationship between bariatric surgery and bone mineral density: a meta-analysis. Obes Surg 26:1414–1421. https://doi.org/10.1007/s11695-015-1928-8
doi: 10.1007/s11695-015-1928-8
pubmed: 26464244
Paccou J, Caiazzo R, Lespessailles E, Cortet B (2022) Bariatric surgery and osteoporosis. Calcif Tissue Int 110:576–591. https://doi.org/10.1007/s00223-020-00798-w
doi: 10.1007/s00223-020-00798-w
pubmed: 33403429
Zibellini J, Seimon RV, Lee CM, Gibson AA, Hsu MS, Shapses SA, Nguyen TV, Sainsbury A (2015) Does diet-induced weight loss lead to bone loss in overweight or obese adults? A systematic review and meta-analysis of clinical trials. J Bone Miner Res 30:2168–2178. https://doi.org/10.1002/jbmr.2564
doi: 10.1002/jbmr.2564
pubmed: 26012544
Muschitz C, Kocijan R, Haschka J, Zendeli A, Pirker T, Geiger C, Müller A, Tschinder B, Kocijan A, Marterer C et al (2016) The impact of vitamin D, calcium, protein supplementation, and physical exercise on bone metabolism after bariatric surgery: the BABS study. J Bone Miner Res 31:672–682. https://doi.org/10.1002/jbmr.2707
doi: 10.1002/jbmr.2707
pubmed: 26350034
Pead MJ, Skerry TM, Lanyon LE (1988) Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J Bone Miner Res 3:647–656. https://doi.org/10.1002/jbmr.5650030610
doi: 10.1002/jbmr.5650030610
pubmed: 3251399
Jagger CJ, Chambers TJ, Chow JW (1995) Stimulation of bone formation by dynamic mechanical loading of rat caudal vertebrae is not suppressed by 3-amino-1-hydroxypropylidene-1-bisphosphonate (AHPrBP). Bone 16:309–313. https://doi.org/10.1016/8756-3282(94)00043-3
doi: 10.1016/8756-3282(94)00043-3
pubmed: 7786634