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Risk Factors for Secondary Hyperparathyroidism After Bariatric Surgery

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Abstract

The frequency of bariatric operations is rising rapidly as is the number of patients on long term follow-up. Therefore, it is important to study the nutritional and metabolic complications and establish preventive measures. Secondary hyperparathyroidism and metabolic bone disease are frequent after bariatric surgery and are caused by the reduced intake and absorption of calcium and vitamin D. Unfortunately, obesity itself poses a risk of vitamin D deficiency and secondary hyperparathyroidism, other risk factors being darker skin colour, increasing age and living at high latitude. These risks are further increased by bariatric surgery the type of operation being the most important risk factor. Purely restrictive operations carry the lowest risk, reduced calcium intake being the main cause for secondary hyperparathyroidism. In malabsorptive operations calcium and vitamin D malabsorption further increase the risk of secondary hyperparathyroidism and osteoporosis. Prevention can be efficiently established by supplementation with calcium and vitamin D dosed according to the degree of malabsorption.

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References

  1. Buchwald H, Oien D. Bariatric/metabolic surgery worldwide 2011. Obes Surg. 2013;23(4):427–36.

    Article  PubMed  Google Scholar 

  2. Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34.

    Article  PubMed  Google Scholar 

  3. Gehrer S, Kern B, Peters T, Christoffel-Courtin C, Peterli R. Fewer nutrient deficiencies after laparoscopic sleeve gastrectomy (LSG) than after laparoscopic Roux-Y-gastric bypass (LRYGB)—a prospective study. Obes Surg. 2010;20(4):447–53.

    Article  PubMed  Google Scholar 

  4. Toelle P, Peterli R, Zobel I, Noppen C, Christoffel-Courtin C, Peters T. Risk factors for secondary hyperparathyroidism after bariatric surgery: a comparison of 4 different operations and of vitamin D-receptor-polymorphism. Exp Clin Endocrinol Diabetes. 2012;120(10):629–34.

    Article  CAS  PubMed  Google Scholar 

  5. Malinowski S. Nutritional and metabolic complications of bariatric surgery. Am J Med Sci. 2006;331(4):219–25.

    Article  PubMed  Google Scholar 

  6. Alvarez J. Nutrient deficiencies secondary to bariatric surgery. Curr Opin Clin Nutr Metab Care. 2004;7(5):569–75.

    Article  Google Scholar 

  7. Mechanick J, Youdim A, Jones B, Garvey W, Hurley D, McMahon M, et al. AACE/TOS/ASMBS Guidelines. Endocr Pract. 2013;19(2):337–72.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Moizé V, Pi-Sunyer X, Mochari H, Vidal J. Nutritional pyramid for post-gastric bypass patients. Obes Surg. 2010;20:1133–41.

    Article  PubMed  Google Scholar 

  9. Schweiger C, Weiss R, Keidar A. Effect of different bariatric operations on food tolerance and quality of eating. Obes Surg. 2010;20:1393–9.

    Article  PubMed  Google Scholar 

  10. Melissas J, Koukouraki S, Askoxylakis J, Stathaki M, Daskalakis M, Perisinakis K, Karkavitsas N. Sleeve gastrectomy: a restrictive procedure? Obes Surg. 2007;17:57–62.

    Article  PubMed  Google Scholar 

  11. Lunt M, Felsenberg D, Adams J, Benevolenskaya L, Cannata J, Dequeker J, et al. Population-based geographic variations in DXA bone density in Europe: the EVOS study. European vertebral osteoporosis. Osteoporos Int. 1997;7(3):175–89.

    Article  CAS  PubMed  Google Scholar 

  12. Gonelli S, Cafarelli C, Nuti R. Obesity and fracture risk. Clin Cases Miner Bone Metab. 2014;11(1):9–14.

    Google Scholar 

  13. Cao J. Effects of obesity on bone metabolism. J Orthop Surg Res. 2011;15(6):30.

    Article  Google Scholar 

  14. Bielohuby M, Matsuura M, Herbach N, Kienzle E, Slawik M, Hoeflich A, Bidlingmaier M. Short-term exposure to low-carbohydrate, high-fat diets induces low bone mineral density and reduces bone formation in rats. J Bone Miner Res. 2010;25(2):275–84.

    Article  CAS  PubMed  Google Scholar 

  15. Grace C, Vincent R, Aylwin S. High prevalence of vitamin D insufficiency in a United Kingdom urban morbidly obese population: implications for testing and treatment. Surg Obes Relat Dis. 2014;10(2):355–60.

    Article  PubMed  Google Scholar 

  16. 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 

  17. Ducloux R, Nobécourt E, Chevallier J, Ducloux H, Elian N, Altman J. Vitamin D deficiency before bariatric surgery: should supplement intake be routinely prescribed? Obes Surg. 2011;21(5):556–60.

    Article  PubMed  Google Scholar 

  18. Yanoff L, Parikh S, Spitalnik A, Denkinger B, Sebring N, Slaughter P, et al. The prevalence of hypovitaminosis D and secondary hyperparathyroidism in obese Black Americans. Clin Endocrinol (Oxf). 2006;64(5):523–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Drincic A, Fuller E, Heaney R, Armas L. 25-Hydroxyvitamin D response to graded vitamin D3 supplementation among obese adults. J Clin Endocrinol Metab. 2013;98(12):4845–51.

    Article  CAS  PubMed  Google Scholar 

  20. Coupaye M, Breuil M, Rivière P, Castel B, Bogard C, Dupré T, et al. Serum vitamin D increases with weight loss in obese subjects 6 months after Roux-en-Y gastric bypass. Obes Surg. 2013;23(4):486–93.

    Article  PubMed  Google Scholar 

  21. Vilarrasa N, de Gordejuela A, Gómez-Vaquero C, Pujol J, Elio I, SanJosé P, et al. Effect of bariatric surgery on bone mineral density: comparison of gastric bypass and sleeve gastrectomy. Obes Surg. 2013;23(12):2086–91.

    Article  PubMed  Google Scholar 

  22. Wucher H, Ciangura C. Effects of weight loss on bone status after bariatric surgery. Obes Surg. 2008;18(1):58–65.

    Article  PubMed  Google Scholar 

  23. von Mach M, 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.

    Article  Google Scholar 

  24. Carlin A, Rao D, Yager K, Genaw J, Parikh N, Szymanski W. Effect of gastric bypass surgery on vitamin D nutritional status. Surg Obes Relat Dis. 2006;2(6):638–42.

    Article  PubMed  Google Scholar 

  25. Ruiz-Tovar J, Oller I, Tomas A, Llavero C, Arroyo A, Calero A, Martinez-Blasco A, Calpena R. Mid-term effects of sleeve gastrectomy on calcium metabolism parameters, vitamin D and parathormone (PTH) in morbid obese women. Obes Surg. 2012;22:797–801.

    Article  PubMed  Google Scholar 

  26. Flores L, Martínez Osaba M, Andreu A. Calcium and vitamin D supplementation after gastric bypass should be individualized to improve or avoid hyperparathyroidism. Obes Surg. 2010;20:738–43.

    Article  PubMed  Google Scholar 

  27. Karefylakis C, Näslund I, Edholm D, Sundbom M, Karlsson F, Rask E. Vitamin D status 10 years after primary gastric bypass: gravely high prevalence of hypovitaminosis D and raised PTH levels. Obes Surg. 2014;24(3):343–88.

    Article  PubMed  Google Scholar 

  28. Hewitt S, Sovik T, Aasheim E, Kristinsson J, Jahnsen J, Birketvedt G, et al. Secondary hyperparathyroidism, vitamin D sufficiency and serum calcium 5 years after gastric bypass and duodenal switch. Obes Surg. 2013;23(3):384–90.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  30. Scibora L, Buchwald H, Petit M, Hughes J, Ikramuddin S. Bone strength is preserved following bariatric surgery. Obes Surg. 2014;. doi:10.1007/s11695-014-1341-8.

    PubMed  Google Scholar 

  31. Yu E, Bouxsein M, Roy A, Baldwin C, Cange A, Neer R, et al. Bone loss after bariatric surgery: discordant results between DXA and QCT bone density. J Bone Miner Res. 2014;29(3):542–50.

    Article  CAS  PubMed  Google Scholar 

  32. Ebelin R. Vitamin D and bone health: epidemiologic studies. Bonekey Rep. 2014;5(3):511.

    Google Scholar 

  33. Pacheco D, Menárguez J, Cristobal E, Arribas B, Alcazar JA, Carrión R, et al. BsmI vitamin D receptor polymorphism and pathogenesis of parathyroid adenoma. Med Sci Monit. 2000;6(4):658–60.

    CAS  PubMed  Google Scholar 

  34. Carling T, Kindmark A, Hellman P, Lundgren E, Ljunghall S, Rastad J, et al. Vitamin D receptor genotypes in primary hyperparathyroidism. Nat Med. 1995;1(12):1309–11.

    Article  CAS  PubMed  Google Scholar 

  35. Rubello D, Giannini S, D’Angelo A, Nobile M, Carraio G, Rigotti P, et al. Secondary hyperparathyroidism is associated with vitamin D receptor polymorphism and bone density after renal transplantation. Biomed Pharmacother. 2005;59(7):402–7.

    Article  CAS  PubMed  Google Scholar 

  36. Falkiewicz K, Bidzińska B, Demissie M, Boratyńska M, Zmonarski SC, Tworowska K, et al. Influence of vitamin D receptor gene polymorphisms on secondary hyperparathyroidism and bone density after kidney transplantation. Transplant Proc. 2005;37(2):1023–5.

    Article  CAS  PubMed  Google Scholar 

  37. Balsa J, Iglesias B, Peromingo R, Conde S, Vazquez C, San-Millan J, et al. Vitamin D receptor polymorphisms in secondary hyperparathyroidism after Scopinaro’s biliopancreatic diversion. Obes Surg. 2010;20(10):1415–21.

    Article  PubMed  Google Scholar 

  38. Hilger J, Friedel A, Herr R, Rausch T, Roos F, Wahl D, et al. A systematic review of vitamin D status in populations worldwide. Br J Nutr. 2014;111(1):23–45.

    Article  CAS  PubMed  Google Scholar 

  39. Ebeling PR, Sandgren ME, DiMagno EP, Lane AW, DeLuca HF, Riggs BL. Evidence of an age related decrease in intestinal responsiveness to vitamin D: relationship between serum 1,25-dihydroxyvitamin D3 and intestinal vitamin D receptor concentrations in normal women. J Clin Endocrinol Metab. 1992;75(1):176–82.

    CAS  PubMed  Google Scholar 

  40. Recker R. Calcium absorption and achlorhydria. N Engl J Med. 1985;313:70–3.

    Article  CAS  PubMed  Google Scholar 

  41. Sipponen P, Härkonen M. Hypochlorhydric stomach: a risk condition for calcium malabsorption and osteoporosis. Scand J Gastroenterol. 2010;45:133–8.

    Article  CAS  PubMed  Google Scholar 

  42. O’Connell M, Madden D, Murray A, Heaney R, Kerzner L. Effects of proton pump inhibitors on calcium carbonate absorption in women: a randomized crossover trial. Am J Med. 2005;118(7):778–81.

    Article  PubMed  Google Scholar 

  43. Yang Y, Lewis J, Epstein S, Metz D. Long-term proton pump inhibitor therapy and risk of hip fracture. JAMA. 2006;296(24):2947–53.

    Article  CAS  PubMed  Google Scholar 

  44. Peterli R, Steinert R, Woelnerhanssen B, Peters T, Christoffel-Courtin C, Gass M, et al. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg. 2012;22(5):740–8.

    Article  PubMed Central  PubMed  Google Scholar 

  45. Khor E, Wee Y, Baldock P. Influence of hormonal appetite and energy regulators on bone. Curr Osteoporos Rep. 2013;11(3):194–202.

    Article  PubMed  Google Scholar 

  46. Misselwitz B, Pohl D, Fruhauf H, Fried M, Vavricka S, Fox M. Lactose malabsorption and intolerance: pathogenesis, diagnosis and treatment. United Eur Gastroenterol J. 2013;1(3):151–9.

    Article  Google Scholar 

  47. Fish E, Beverstein G, Olson D, Reinhardt S, Garren M, Gould J. Vitamin D status of morbidly obese bariatric surgery patients. J Surg Res. 2010;164(2):198–202.

    Article  CAS  PubMed  Google Scholar 

  48. Bächler T, Schiesser M, Lutz T, le Roux C, Bueter M. Where to begin and where to end? Preoperative assessment for patients undergoing metabolic surgery. Dig Surg. 2014;31(1):25–32.

    Article  PubMed  Google Scholar 

  49. Aills L, Blankenship J, Buffington C, Furtado M, Parrot J, Allied Health Sciences Section ad Hoc Nutrition Committee. ASMBS allied health nutritional guidelines for the surgical weight loss patient. Surg Obes Relat Dis. 2008;5(Suppl 4):73–108.

    Article  Google Scholar 

  50. Xanthakos S. Nutritional deficiencies in obesity and after bariatric surgery. Pediatr Clin North Am. 2009;56(5):1105–21.

    Article  PubMed Central  PubMed  Google Scholar 

  51. Li K, Kaaks R, Linseisen J, Rohrmann. S. Associations of dietary calcium intake and calcium supplementation with myocardial infarction and stroke risk and overall cardiovascular mortality in the Heidelberg cohort of the European Prospective Investigation into Cancer and Nutrition study (EPIC-Heidelberg). Heart. 2012;98:920–5.

    Article  CAS  PubMed  Google Scholar 

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Disclosures

Conflict of interest

T. Peters, P. Toelle, M. Gebhart, M. Slawik declare that they have no conflict of interest.

Animal/Human Studies

This article does not contain any studies with human or animal subjects performed by any of the authors.

Ethical Standard

All authors declare that all studies they were involved in this publication comply with the ethical standards of the responsible institutional and national committees and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients.

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Peters, T., Toelle, P., Gebhart, M. et al. Risk Factors for Secondary Hyperparathyroidism After Bariatric Surgery. Clinic Rev Bone Miner Metab 12, 228–233 (2014). https://doi.org/10.1007/s12018-014-9173-6

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