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Bariatric Surgery and Effects on Calcium and Bone Metabolism

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Abstract

With the increasing epidemic of obesity in the United States as well as abroad, bariatric surgery has emerged as the most effective and sustained treatment for reduction. This treatment modality has been well recognized to diminish the risk of cardiovascular morbidity and mortality and ameliorate diabetes mellitus. However, with time, derangement in mineral metabolism has emerged as a major complication in this population. Population-based study has shown increased prevalence of bone fractures and kidney stone formation following bariatric surgery. The risk appears to be more specific after Roux-en-Y gastric bypass procedures, the most common surgical approach among this population. Over the past decade, there have been advances in the understanding of pathophysiologic mechanisms of both bone loss and kidney stone disease in these patients. The understanding of these underlying pathophysiologic mechanisms may lead to the development of drug therapies that ameliorate this complication. Unfortunately, at the present time, there is no hard data on any specific treatment showing decreased incidence of fragility fractures or kidney stone passage. However, some studies suggest that calcium and vitamin D supplementation may decrease bone loss and bone turnover, and as a result, increase bone mineral density in this population. However, there is concern with the development of kidney stone formation following such an approach. A novel treatment approach would be the use of effervescent potassium calcium citrate that not only prevents complications of bone loss but may diminish the risk of kidney stone formation. Despite preliminary results showing the effectiveness of this drug in the reduction in the parathyroid hormone, bone turnover, and improvement in the urinary saturation marker showing effectiveness against calcium oxalate and uric acid stones, there is no hard data available to support the effectiveness of this treatment in the reduction in fragility fractures or kidney stone incidence. Such studies to explore this effect must be considered in the future.

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References

  1. Adams TD, Gress RE, Smith SC, Halverson RC, Simper SC, Rosamond WD, et al. Long-term mortality after gastric bypass surgery. N Engl J Med. 2007;357(8):753–61. doi:10.1056/NEJMoa066603.

    CAS  PubMed  Google Scholar 

  2. Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA. 2002;288(22):2793–6.

    PubMed  Google Scholar 

  3. Sjostrom L, Narbro K, Sjostrom CD, Karason K, Larsson B, Wedel H, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007;357(8):741–52. doi:10.1056/NEJMoa066254.

    PubMed  Google Scholar 

  4. Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999–2000. JAMA. 2002;288(14):1723–7.

    PubMed  Google Scholar 

  5. Yanovski SZ, Yanovski JA. Obesity. N Engl J Med. 2002;346(8):591–602. doi:10.1056/NEJMra012586.

    CAS  PubMed  Google Scholar 

  6. Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351(26):2683–93. doi:10.1056/NEJMoa035622.

    PubMed  Google Scholar 

  7. Balsiger BM, Murr MM, Poggio JL, Sarr MG. Bariatric surgery. Surgery for weight control in patients with morbid obesity. Med Clin North Am. 2000;84(2):477–89.

    CAS  PubMed  Google Scholar 

  8. Halverson JD, Wise L, Wazna MF, Ballinger WF. Jejunoileal bypass for morbid obesity. A critical appraisal. Am J Med. 1978;64(3):461–75.

    CAS  PubMed  Google Scholar 

  9. Scopinaro N, Gianetta E, Adami GF, Friedman D, Traverso E, Marinari GM, et al. Biliopancreatic diversion for obesity at eighteen years. Surgery. 1996;119(3):261–8.

    CAS  PubMed  Google Scholar 

  10. Scopinaro N, Marinari GM, Camerini G. Laparoscopic standard biliopancreatic diversion: technique and preliminary results. Obes Surg. 2002;12(2):241–4. doi:10.1381/096089202762552692.

    PubMed  Google Scholar 

  11. Deitel M, Shahi B, Anand PK, Deitel FH, Cardinell DL. Long-term outcome in a series of jejunoileal bypass patients. Obes Surg. 1993;3(3):247–52. doi:10.1381/096089293765559250.

    PubMed  Google Scholar 

  12. Steinbrook R. Surgery for severe obesity. N Engl J Med. 2004;350(11):1075–9. doi:10.1056/NEJMp048029.

    CAS  PubMed  Google Scholar 

  13. Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, Pothier CE, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012;366(17):1567–76. doi:10.1056/NEJMoa1200225.

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Leccesi L, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366(17):1577–85. doi:10.1056/NEJMoa1200111.

    CAS  PubMed  Google Scholar 

  15. Mahdy T, Atia S, Farid M, Adulatif A. Effect of Roux-en Y gastric bypass on bone metabolism in patients with morbid obesity: Mansoura experiences. Obes Surg. 2008;18(12):1526–31. doi:10.1007/s11695-008-9653-1.

    PubMed  Google Scholar 

  16. De Prisco C, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci. 2005;329(2):57–61.

    PubMed  Google Scholar 

  17. Fleischer J, Stein EM, Bessler M, Della Badia M, Restuccia N, Olivero-Rivera L, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab. 2008;93(10):3735–40. doi:10.1210/jc.2008-0481.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. 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. J Clin Endocrinol Metab. 2004;89(3):1061–5.

    CAS  PubMed  Google Scholar 

  19. Vilarrasa N, San Jose P, Garcia I, Gomez-Vaquero C, Miras PM, de Gordejuela AG, et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obes Surg. 2011;21(4):465–72. doi:10.1007/s11695-010-0338-1.

    PubMed  Google Scholar 

  20. Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B, et al. Bariatric surgery results in cortical bone loss. J Clin Endocrinol Metab. 2013;98(2):541–9. doi:10.1210/jc.2012-2394.

    CAS  PubMed Central  PubMed  Google Scholar 

  21. Matlaga BR, Shore AD, Magnuson T, Clark JM, Johns R, Makary MA. Effect of gastric bypass surgery on kidney stone disease. J Urol. 2009;181(6):2573–7. doi:10.1016/j.juro.2009.02.029.

    PubMed  Google Scholar 

  22. Nelson WK, Houghton SG, Milliner DS, Lieske JC, Sarr MG. Enteric hyperoxaluria, nephrolithiasis, and oxalate nephropathy: potentially serious and unappreciated complications of Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2005;1(5):481–5. doi:10.1016/j.soard.2005.07.002.

    PubMed  Google Scholar 

  23. Sinha MK, Collazo-Clavell ML, Rule A, Milliner DS, Nelson W, Sarr MG, et al. Hyperoxaluric nephrolithiasis is a complication of Roux-en-Y gastric bypass surgery. Kidney Int. 2007;72(1):100–7. doi:10.1038/sj.ki.5002194.

    CAS  PubMed  Google Scholar 

  24. Asplin JR, Coe FL. Hyperoxaluria in kidney stone formers treated with modern bariatric surgery. J Urol. 2007;177(2):565–9. doi:10.1016/j.juro.2006.09.033.

    PubMed  Google Scholar 

  25. Park AM, Storm DW, Fulmer BR, Still CD, Wood GC, Hartle JE 2nd. A prospective study of risk factors for nephrolithiasis after Roux-en-Y gastric bypass surgery. J Urol. 2009;182(5):2334–9. doi:10.1016/j.juro.2009.07.044.

    CAS  PubMed  Google Scholar 

  26. Duffey BG, Pedro RN, Makhlouf A, Kriedberg C, Stessman M, Hinck B, et al. Roux-en-Y gastric bypass is associated with early increased risk factors for development of calcium oxalate nephrolithiasis. J Am Coll Surg. 2008;206(3):1145–53. doi:10.1016/j.jamcollsurg.2008.01.015.

    PubMed  Google Scholar 

  27. Berarducci A, Haines K, Murr MM. Incidence of bone loss, falls, and fractures after Roux-en-Y gastric bypass for morbid obesity. Appl Nurs Res. 2009;22(1):35–41. doi:10.1016/j.apnr.2007.03.004.

    PubMed  Google Scholar 

  28. Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codoceo J, et al. Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obes Surg. 2009;19(1):41–6. doi:10.1007/s11695-008-9638-0.

    PubMed  Google Scholar 

  29. Pereira FA, de Castro JA, dos Santos JE, Foss MC, Paula FJ. Impact of marked weight loss induced by bariatric surgery on bone mineral density and remodeling. Braz J Med Biol Res. 2007;40(4):509–17.

    CAS  PubMed  Google Scholar 

  30. von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U. Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism. 2004;53(7):918–21.

    Google Scholar 

  31. Goode LR, Brolin RE, Chowdhury HA, Shapses SA. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res. 2004;12(1):40–7. doi:10.1038/oby.2004.7.

    CAS  PubMed  Google Scholar 

  32. Bano G, Rodin DA, Pazianas M, Nussey SS. Reduced bone mineral density after surgical treatment for obesity. Int J Obes Relat Metab Disord. 1999;23(4):361–5.

    CAS  PubMed  Google Scholar 

  33. 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. Obes Surg. 2003;13(3):383–8. doi:10.1381/096089203765887705.

    PubMed  Google Scholar 

  34. Cundy T, Evans MC, Kay RG, Dowman M, Wattie D, Reid IR. Effects of vertical-banded gastroplasty on bone and mineral metabolism in obese patients. Br J Surg. 1996;83(10):1468–72.

    CAS  PubMed  Google Scholar 

  35. Marceau P, Biron S, Lebel S, Marceau S, Hould FS, Simard S, et al. Does bone change after biliopancreatic diversion? J Gastrointest Surg. 2002;6(5):690–8.

    PubMed  Google Scholar 

  36. Moreiro J, Ruiz O, Perez G, Salinas R, Urgeles JR, Riesco M, et al. Parathyroid hormone and bone marker levels in patients with morbid obesity before and after biliopancreatic diversion. Obes Surg. 2007;17(3):348–54. doi:10.1007/s11695-007-9063-9.

    CAS  PubMed  Google Scholar 

  37. Felson DT, Zhang Y, Hannan MT, Anderson JJ. Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res. 1993;8(5):567–73. doi:10.1002/jbmr.5650080507.

    CAS  PubMed  Google Scholar 

  38. Schoenau E, Frost HM. The “muscle-bone unit” in children and adolescents. Calcif Tissue Int. 2002;70(5):405–7. doi:10.1007/s00223-001-0048-8.

    CAS  PubMed  Google Scholar 

  39. Maimoun L, Fattal C, Micallef JP, Peruchon E, Rabischong P. Bone loss in spinal cord-injured patients: from physiopathology to therapy. Spinal Cord. 2006;44(4):203–10. doi:10.1038/sj.sc.3101832.

    CAS  PubMed  Google Scholar 

  40. Zerwekh JE, Ruml LA, Gottschalk F, Pak CY. The effects of twelve weeks of bed rest on bone histology, biochemical markers of bone turnover, and calcium homeostasis in eleven normal subjects. J Bone Miner Res. 1998;13(10):1594–601. doi:10.1359/jbmr.1998.13.10.1594.

    CAS  PubMed  Google Scholar 

  41. Suva LJ. Sclerostin and the unloading of bone. J Bone Miner Res. 2009;24(10):1649–50. doi:10.1359/jbmr.090815.

    CAS  PubMed  Google Scholar 

  42. Schneider V, Oganov V, LeBlanc A, Rakmonov A, Taggart L, Bakulin A, et al. Bone and body mass changes during space flight. Acta Astronaut. 1995;36(8–12):463–6.

    CAS  PubMed  Google Scholar 

  43. Lin C, Jiang X, Dai Z, Guo X, Weng T, Wang J, et al. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. J Bone Miner Res. 2009;24(10):1651–61. doi:10.1359/jbmr.090411.

    CAS  PubMed  Google Scholar 

  44. Day TF, Guo X, Garrett-Beal L, Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell. 2005;8(5):739–50. doi:10.1016/j.devcel.2005.03.016.

    CAS  PubMed  Google Scholar 

  45. Compher CW, Badellino KO, Boullata JI. Vitamin D and the bariatric surgical patient: a review. Obes Surg. 2008;18(2):220–4. doi:10.1007/s11695-007-9289-6.

    PubMed  Google Scholar 

  46. Earthman CP, Beckman LM, Masodkar K, Sibley SD. The link between obesity and low circulating 25-hydroxyvitamin D concentrations: considerations and implications. Int J Obes. 2012;36(3):387–96. doi:10.1038/ijo.2011.119.

    CAS  Google Scholar 

  47. Wortsman J, Matsuoka LY, Chen TC, Lu Z, Holick MF. Decreased bioavailability of vitamin D in obesity. Am J Clin Nutr. 2000;72(3):690–3.

    CAS  PubMed  Google Scholar 

  48. Grethen E, McClintock R, Gupta CE, Jones R, Cacucci BM, Diaz D, et al. Vitamin D and hyperparathyroidism in obesity. J Clin Endocrinol Metab. 2011;96(5):1320–6. doi:10.1210/jc.2010-2202.

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Stein EM, Strain G, Sinha N, Ortiz D, Pomp A, Dakin G, et al. Vitamin D insufficiency prior to bariatric surgery: risk factors and a pilot treatment study. Clin Endocrinol. 2009;71(2):176–83. doi:10.1111/j.1365-2265.2008.03470.x.

    CAS  Google Scholar 

  50. Avgerinos DV, Leitman IM, Martinez RE, Liao EP. Evaluation of markers for calcium homeostasis in a population of obese adults undergoing gastric bypass operations. J Am Coll Surg. 2007;205(2):294–7. doi:10.1016/j.jamcollsurg.2007.02.078.

    PubMed  Google Scholar 

  51. Pugnale N, Giusti V, Suter M, Zysset E, Heraief E, Gaillard RC, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes Relat Metab Disord. 2003;27(1):110–6. doi:10.1038/sj.ijo.0802177.

    CAS  PubMed  Google Scholar 

  52. Youssef Y, Richards WO, Sekhar N, Kaiser J, Spagnoli A, Abumrad N, et al. Risk of secondary hyperparathyroidism after laparoscopic gastric bypass surgery in obese women. Surg Endosc. 2007;21(8):1393–6. doi:10.1007/s00464-007-9228-6.

    CAS  PubMed  Google Scholar 

  53. Valderas JP, Velasco S, Solari S, Liberona Y, Viviani P, Maiz A, et al. Increase of bone resorption and the parathyroid hormone in postmenopausal women in the long-term after Roux-en-Y gastric bypass. Obes Surg. 2009;19(8):1132–8. doi:10.1007/s11695-009-9890-y.

    PubMed  Google Scholar 

  54. Riedt CS, Brolin RE, Sherrell RM, Field MP, Shapses SA. True fractional calcium absorption is decreased after Roux-en-Y gastric bypass surgery. Obesity. 2006;14(11):1940–8. doi:10.1038/oby.2006.226.

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Williams SE. Metabolic bone disease in the bariatric surgery patient. J Obes. 2011;2011:634614. doi:10.1155/2011/634614.

    PubMed Central  PubMed  Google Scholar 

  56. Johnson JM, Maher JW, DeMaria EJ, Downs RW, Wolfe LG, Kellum JM. The long-term effects of gastric bypass on vitamin D metabolism. Ann Surg. 2006;243(5):701–4; discussion 4–5. doi:10.1097/01.sla.0000216773.47825.c1.

    Google Scholar 

  57. El-Kadre LJ, Rocha PR, de Almeida Tinoco ac, Tinoco Rc. Calcium metabolism in pre- and postmenopausal morbidly obese women at baseline and after laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2004;14(8):1062–6. doi:10.1381/0960892041975505.

    PubMed  Google Scholar 

  58. Madan AK, Orth WS, Tichansky DS, Ternovits CA. Vitamin and trace mineral levels after laparoscopic gastric bypass. Obes Surg. 2006;16(5):603–6. doi:10.1381/096089206776945057.

    PubMed  Google Scholar 

  59. Khandalavala BN, Hibma PP, Fang X. Prevalence and persistence of vitamin D deficiency in biliopancreatic diversion patients: a retrospective study. Obes Surg. 2010;20(7):881–4. doi:10.1007/s11695-010-0185-0.

    PubMed  Google Scholar 

  60. Aarts EO, Janssen IM, Berends FJ. The gastric sleeve: losing weight as fast as micronutrients? Obes Surg. 2011;21(2):207–11. doi:10.1007/s11695-010-0316-7.

    PubMed Central  PubMed  Google Scholar 

  61. Balsa JA, Botella-Carretero JI, Peromingo R, Caballero C, Munoz-Malo T, Villafruela JJ, et al. Chronic increase of bone turnover markers after biliopancreatic diversion is related to secondary hyperparathyroidism and weight loss. Relation with bone mineral density. Obes Surg. 2010;20(4):468–73. doi:10.1007/s11695-009-0028-z.

    PubMed  Google Scholar 

  62. Wucher H, Ciangura C, Poitou C, Czernichow S. Effects of weight loss on bone status after bariatric surgery: association between adipokines and bone markers. Obes Surg. 2008;18(1):58–65. doi:10.1007/s11695-007-9258-0.

    PubMed  Google Scholar 

  63. Garcia de la Torre N, Rubio MA, Bordiu E, Cabrerizo L, Aparicio E, Hernandez C et al. Effects of weight loss after bariatric surgery for morbid obesity on vascular endothelial growth factor-A, adipocytokines, and insulin. J Clin Endocrinol Metab. 2008;93(11):4276–81. doi:10.1210/jc.2007-1370.

    Google Scholar 

  64. Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17(9):1563–9. doi:10.1359/jbmr.2002.17.9.1563.

    CAS  PubMed  Google Scholar 

  65. Karsenty G, Oury F. The central regulation of bone mass, the first link between bone remodeling and energy metabolism. J Clin Endocrinol Metab. 2010;95(11):4795–801. doi:10.1210/jc.2010-1030.

    CAS  PubMed  Google Scholar 

  66. Yadav VK, Oury F, Suda N, Liu ZW, Gao XB, Confavreux C, et al. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell. 2009;138(5):976–89. doi:10.1016/j.cell.2009.06.051.

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Karsenty G. Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab. 2006;4(5):341–8. doi:10.1016/j.cmet.2006.10.008.

    CAS  PubMed  Google Scholar 

  68. Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM, et al. Serum markers of bone turnover are increased at six and 18 months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocrinol Metab. 2010;95(1):159–66. doi:10.1210/jc.2009-0265.

    CAS  PubMed Central  PubMed  Google Scholar 

  69. Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res. 2006;21(10):1648–56. doi:10.1359/jbmr.060707.

    CAS  PubMed  Google Scholar 

  70. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest. 2007;117(1):13–23. doi:10.1172/JCI30227.

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Tymitz K, Engel A, McDonough S, Hendy MP, Kerlakian G. Changes in ghrelin levels following bariatric surgery: review of the literature. Obes Surg. 2011;21(1):125–30. doi:10.1007/s11695-010-0311-z.

    PubMed  Google Scholar 

  72. Huda MS, Dovey T, Wong SP, English PJ, Halford J, McCulloch P, et al. Ghrelin restores ‘lean-type’ hunger and energy expenditure profiles in morbidly obese subjects but has no effect on postgastrectomy subjects. Int J Obes. 2009;33(3):317–25. doi:10.1038/ijo.2008.270.

    CAS  Google Scholar 

  73. Garcia-Fuentes E, Garrido-Sanchez L, Garcia-Almeida JM, Garcia-Arnes J, Gallego-Perales JL, Rivas-Marin J, et al. Different effect of laparoscopic Roux-en-Y gastric bypass and open biliopancreatic diversion of Scopinaro on serum PYY and ghrelin levels. Obes Surg. 2008;18(11):1424–9. doi:10.1007/s11695-008-9560-5.

    CAS  PubMed  Google Scholar 

  74. Reinehr T, Roth CL, Schernthaner GH, Kopp HP, Kriwanek S, Schernthaner G. Peptide YY and glucagon-like peptide-1 in morbidly obese patients before and after surgically induced weight loss. Obes Surg. 2007;17(12):1571–7. doi:10.1007/s11695-007-9323-8.

    PubMed  Google Scholar 

  75. Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK. Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy: a prospective, double blind study. Ann Surg. 2008;247(3):401–7. doi:10.1097/SLA.0b013e318156f012.

    PubMed  Google Scholar 

  76. Bollag RJ, Zhong Q, Phillips P, Min L, Zhong L, Cameron R, et al. Osteoblast-derived cells express functional glucose-dependent insulinotropic peptide receptors. Endocrinology. 2000;141(3):1228–35.

    CAS  PubMed  Google Scholar 

  77. Nuche-Berenguer B, Moreno P, Esbrit P, Dapia S, Caeiro JR, Cancelas J, et al. Effect of GLP-1 treatment on bone turnover in normal, type 2 diabetic, and insulin-resistant states. Calcif Tissue Int. 2009;84(6):453–61. doi:10.1007/s00223-009-9220-3.

    CAS  PubMed  Google Scholar 

  78. Grodin JM, Siiteri PK, MacDonald PC. Source of estrogen production in postmenopausal women. J Clin Endocrinol Metab. 1973;36(2):207–14.

    CAS  PubMed  Google Scholar 

  79. Hammoud A, Gibson M, Hunt SC, Adams TD, Carrell DT, Kolotkin RL, et al. Effect of Roux-en-Y gastric bypass surgery on the sex steroids and quality of life in obese men. J Clin Endocrinol Metab. 2009;94(4):1329–32. doi:10.1210/jc.2008-1598.

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Gallagher JC, Riggs BL, DeLuca HF. Effect of estrogen on calcium absorption and serum vitamin D metabolites in postmenopausal osteoporosis. J Clin Endocrinol Metab. 1980;51(6):1359–64.

    CAS  PubMed  Google Scholar 

  81. Durrani O, Morrisroe S, Jackman S, Averch T. Analysis of stone disease in morbidly obese patients undergoing gastric bypass surgery. J Endourol. 2006;20(10):749–52. doi:10.1089/end.2006.20.749.

    PubMed  Google Scholar 

  82. Semins MJ, Matlaga BR, Shore AD, Steele K, Magnuson T, Johns R, et al. The effect of gastric banding on kidney stone disease. Urology. 2009;74(4):746–9. doi:10.1016/j.urology.2009.04.093.

    PubMed Central  PubMed  Google Scholar 

  83. Duffey BG, Alanee S, Pedro RN, Hinck B, Kriedberg C, Ikramuddin S, et al. Hyperoxaluria is a long-term consequence of Roux-en-Y Gastric bypass: a 2-year prospective longitudinal study. J Am Coll Surg. 2010;211(1):8–15. doi:10.1016/j.jamcollsurg.2010.03.007.

    PubMed  Google Scholar 

  84. Patel BN, Passman CM, Fernandez A, Asplin JR, Coe FL, Kim SC, et al. Prevalence of hyperoxaluria after bariatric surgery. J Urol. 2009;181(1):161–6. doi:10.1016/j.juro.2008.09.028.

    PubMed Central  PubMed  Google Scholar 

  85. Kumar R, Lieske JC, Collazo-Clavell ML, Sarr MG, Olson ER, Vrtiska TJ, et al. Fat malabsorption and increased intestinal oxalate absorption are common after Roux-en-Y gastric bypass surgery. Surgery. 2011;149(5):654–61. doi:10.1016/j.surg.2010.11.015.

    PubMed Central  PubMed  Google Scholar 

  86. Requarth JA, Burchard KW, Colacchio TA, Stukel TA, Mott LA, Greenberg ER, et al. Long-term morbidity following jejunoileal bypass. The continuing potential need for surgical reversal. Arch Surg. 1995;130(3):318–25.

    CAS  PubMed  Google Scholar 

  87. Ferraz RR, Tiselius HG, Heilberg IP. Fat malabsorption induced by gastrointestinal lipase inhibitor leads to an increase in urinary oxalate excretion. Kidney Int. 2004;66(2):676–82. doi:10.1111/j.1523-1755.2004.00790.x.

    CAS  PubMed  Google Scholar 

  88. Odstrcil EA, Martinez JG, Santa Ana CA, Xue B, Schneider RE, Steffer KJ, et al. The contribution of malabsorption to the reduction in net energy absorption after long-limb Roux-en-Y gastric bypass. Am J Clin Nutr. 2010;92(4):704–13. doi:10.3945/ajcn.2010.29870.

    CAS  PubMed  Google Scholar 

  89. Li JV, Ashrafian H, Bueter M, Kinross J, Sands C, le Roux CW, et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut. 2011;60(9):1214–23. doi:10.1136/gut.2010.234708.

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Kaufman DW, Kelly JP, Curhan GC, Anderson TE, Dretler SP, Preminger GM, et al. Oxalobacter formigenes may reduce the risk of calcium oxalate kidney stones. J Am Soc Nephrol. 2008;19(6):1197–203. doi:10.1681/ASN.2007101058.

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Freel RW, Hatch M, Earnest DL, Goldner AM. Oxalate transport across the isolated rat colon. A re-examination. Biochim Biophys Acta. 1980;600(3):838–43.

    CAS  PubMed  Google Scholar 

  92. Dobbins JW, Binder HJ. Effect of bile salts and fatty acids on the colonic absorption of oxalate. Gastroenterology. 1976;70(6):1096–100.

    CAS  PubMed  Google Scholar 

  93. Maalouf NM, Tondapu P, Guth ES, Livingston EH, Sakhaee K. Hypocitraturia and hyperoxaluria after Roux-en-Y gastric bypass surgery. J Urol. 2010;183(3):1026–30. doi:10.1016/j.juro.2009.11.022.

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Froeder L, Arasaki CH, Malheiros CA, Baxmann AC, Heilberg IP. Response to dietary oxalate after bariatric surgery. Clin J Am Soc Nephrol. 2012;7(12):2033–40. doi:10.2215/CJN.02560312.

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Alpern RJ, Sakhaee K. The clinical spectrum of chronic metabolic acidosis: homeostatic mechanisms produce significant morbidity. Am J Kidney Dis. 1997;29(2):291–302.

    CAS  PubMed  Google Scholar 

  96. Semins MJ, Asplin JR, Steele K, Assimos DG, Lingeman JE, Donahue S, et al. The effect of restrictive bariatric surgery on urinary stone risk factors. Urology. 2010;76(4):826–9. doi:10.1016/j.urology.2010.01.037.

    PubMed  Google Scholar 

  97. Penniston KL, Kaplon DM, Gould JC, Nakada SY. Gastric band placement for obesity is not associated with increased urinary risk of urolithiasis compared to bypass. J Urol. 2009;182(5):2340–6. doi:10.1016/j.juro.2009.07.041.

    CAS  PubMed  Google Scholar 

  98. Tondapu P, Provost D, Adams-Huet B, Sims T, Chang C, Sakhaee K. Comparison of the absorption of calcium carbonate and calcium citrate after Roux-en-Y gastric bypass. Obes Surg. 2009;19(9):1256–61. doi:10.1007/s11695-009-9850-6.

    CAS  PubMed  Google Scholar 

  99. Mechanick JI, Kushner RF, Sugerman HJ, Gonzalez-Campoy JM, Collazo-Clavell ML, Guven S, et al. American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic AND Bariatric Surgery Medical Guidelines for Clinical Practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Surg Obes Relat Dis. 2008;4(5 Suppl):S109–84. doi:10.1016/j.soard.2008.08.009.

    PubMed  Google Scholar 

  100. Heller HJ, Greer LG, Haynes SD, Poindexter JR, Pak CY. Pharmacokinetic and pharmacodynamic comparison of two calcium supplements in postmenopausal women. J Clin Pharmacol. 2000;40(11):1237–44.

    CAS  PubMed  Google Scholar 

  101. Harvey JA, Kenny P, Poindexter J, Pak CY. Superior calcium absorption from calcium citrate than calcium carbonate using external forearm counting. J Am Coll Nutr. 1990;9(6):583–7.

    CAS  PubMed  Google Scholar 

  102. Pak CY, Avioli LV. Factors affecting absorbability of calcium from calcium salts and food. Calcif Tissue Int. 1988;43(2):55–60.

    CAS  PubMed  Google Scholar 

  103. Sakhaee K, Pak C. Superior calcium bioavailability of effervescent potassium calcium citrate over tablet formulation of calcium citrate after Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2011;. doi:10.1016/j.soard.2011.11.011.

    Google Scholar 

  104. Sakhaee K, Griffith C, Pak CY. Biochemical control of bone loss and stone-forming propensity by potassium-calcium citrate after bariatric surgery. Surg Obes Relat Dis. 2012;8(1):67–72. doi:10.1016/j.soard.2011.05.001.

    PubMed  Google Scholar 

  105. Rosen CJ, Brown S. Severe hypocalcemia after intravenous bisphosphonate therapy in occult vitamin D deficiency. N Engl J Med. 2003;348(15):1503–4. doi:10.1056/NEJM200304103481521.

    PubMed  Google Scholar 

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Acknowledgments

The author would like to acknowledge Ashlei L. Johnson for her role in the editorial process of this manuscript.

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Khashayar Sakhaee declares that he has no conflict of interest.

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  1. Department of Internal Medicine, University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Boulevard, Dallas, TX, 75390-8885, USA

    Khashayar Sakhaee

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Sakhaee, K. Bariatric Surgery and Effects on Calcium and Bone Metabolism. Clinic Rev Bone Miner Metab 12, 240–251 (2014). https://doi.org/10.1007/s12018-013-9145-2

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