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The Relation Between Bone and Stone Formation

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Abstract

Hypercalciuria is the most common metabolic abnormality found in patients with calcium-containing kidney stones. Patients with hypercalciuria often excrete more calcium than they absorb, indicating a net loss of total-body calcium. The source of this additional urinary calcium is almost certainly the skeleton, the largest repository of calcium in the body. Hypercalciuric stone formers exhibit decreased bone mineral density (BMD), which is correlated with the increase in urine calcium excretion. The decreased BMD also correlates with an increase in markers of bone turnover as well as increased fractures. In humans, it is difficult to determine the cause of the decreased BMD in hypercalciuric stone formers. To study the effect of hypercalciuria on bone, we utilized our genetic hypercalciuric stone-forming (GHS) rats, which were developed through successive inbreeding of the most hypercalciuric Sprague-Dawley rats. GHS rats excrete significantly more urinary calcium than similarly fed controls, and all the GHS rats form kidney stones while control rats do not. The hypercalciuria is due to a systemic dysregulation of calcium homeostasis, with increased intestinal calcium absorption, enhanced bone mineral resorption, and decreased renal tubule calcium reabsorption associated with an increase in vitamin D receptors in all these target tissues. We recently found that GHS rats fed an ample calcium diet have reduced BMD and that their bones are more fracture-prone, indicating an intrinsic disorder of bone not secondary to diet. Using this model, we should better understand the pathogenesis of hypercalciuria and stone formation in humans to ultimately improve the bone health of patients with kidney stones.

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References

  1. Monk RD, Bushinsky DA (2011) Kidney stones. In: Kronenberg HM, Melmed S, Polonsky KS, Larsen PR (eds) Williams textbook of endocrinology. WB Saunders, Philadelphia, pp 1350–1367

    Chapter  Google Scholar 

  2. Bushinsky DA, Coe FL, Moe OW (2012) Nephrolithiasis. In: Brenner BM (ed) The kidney. WB Saunders, Philadelphia, pp 1455–1507

    Google Scholar 

  3. Worcester EM, Coe FL (2010) Calcium kidney stones. N Engl J Med 363:954–963

    Article  PubMed  CAS  Google Scholar 

  4. Bushinsky DA, Moe OW (2012) Calcium stones. In: De Broe ME (ed) Oxford textbook of clinical nephrology. Oxford University Press, Oxford

    Google Scholar 

  5. Bushinsky DA (2002) Recurrent hypercalciuric nephrolithiasis—does diet help? N Engl J Med 346:124–125

    Article  PubMed  Google Scholar 

  6. Pak CYC (1992) Pathophysiology of calcium nephrolithiasis. In: Seldin DW, Giebisch G (eds) The kidney: physiology and pathophysiology. Raven Press, New York, pp 2461–2480

    Google Scholar 

  7. Asplin JR, Bauer KA, Kinder J, Muller G, Coe BJ, Parks JH, Coe FL (2003) Bone mineral density and urine calcium excretion among subjects with and without nephrolithiasis. Kidney Int 63:662–669

    Article  PubMed  CAS  Google Scholar 

  8. Pacifici R, Rothstein M, Rifas L et al (1990) Increased monocyte interleukin-1 activity and decreased vertebral bone density in patients with fasting idiopathic hypercalciuria. J Clin Endocrinol Metab 71:138–145

    Article  PubMed  CAS  Google Scholar 

  9. Pietschmann F, Breslau NA, Pak CYC (1992) Reduced vertebral bone density in hypercalciuric nephrolithiasis. J Bone Miner Res 7:1383–1388

    Article  PubMed  CAS  Google Scholar 

  10. Vezzoli G, Soldati L, Ardila M et al (2005) Urinary calcium is a determinant of bone mineral density in elderly men participating in the InCHIANTI study. Kidney Int 67:2006–2014

    Article  PubMed  Google Scholar 

  11. Giannini S, Nobile M, Dalle Carbonare L et al (2003) Hypercalciuria is a common and important finding in postmenopausal women with osteoporosis. Eur J Endocrinol 149:209–213

    Article  PubMed  CAS  Google Scholar 

  12. Jaeger P, Lippuner K, Casez JP, Hess B, Ackerman D, Hug C (1994) Low bone mass in idiopathic renal stone formers: magnitude and significance. J Bone Miner Res 9:1525–1532

    Article  PubMed  CAS  Google Scholar 

  13. Giannini S, Nobile M, Sartori L, Calo L, Tasca A, Dalle Carbonare L, Ciuffreda M, D’Angelo A, Pagano F, Crepaldi G (1998) Bone density and skeletal metabolism are altered in idiopathic hypercalciuria. Clin Nephrol 50:94–100

    PubMed  CAS  Google Scholar 

  14. Misael da Silva AM, dos Reis LM, Pereira RC, Futata E, Branco-Martins CT, Noronha IL, Wajchemberg BL, Jorgetti V (2002) Bone involvement in idiopathic hypercalciuria. Clin Nephrol 57:183–191

    Article  PubMed  CAS  Google Scholar 

  15. Tasca A, Cacciola A, Ferrarese P, Ioverno E, Visona E, Bernardi C, Nobile M, Giannini S (2002) Bone alterations in patients with idiopathic hypercalciuria and calcium nephrolithiasis. Urology 59:865–869

    Article  PubMed  CAS  Google Scholar 

  16. Heilberg IP, Weisinger JR (2006) Bone disease in idiopathic hypercalciuria. Curr Opin Nephrol Hypertens 15:394–402

    Article  PubMed  CAS  Google Scholar 

  17. Lauderdale DS, Thisted RA, Wen M, Favus M (2001) Bone mineral density and fracture among prevalent kidney stone cases in the Third National Health and Nutrition Examination Survey. J Bone Miner 16:1893–1898

    Article  CAS  Google Scholar 

  18. Cauley JA, Blackwell T, Zmuda JM, Fullman RL, Ensrud KE, Stone KL, Barrett-Connor E, Orwoll ES (2010) Correlates of trabecular and cortical volumetric bone mineral density at the femoral neck and lumbar spine: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 25:1958–1971

    Article  PubMed  Google Scholar 

  19. Urivetzky M, Anna PS, Smith AD (1988) Plasma osteocalcin levels in stone disease: a potential aid in the differential diagnosis of calcium nephrolithiasis. J Urol 139:12–14

    PubMed  CAS  Google Scholar 

  20. Liberman UA, Sperling O, Atsmon A, Frank M, Modan M, deVries A (1968) Metabolic and calcium kinetic studies in idiopathic hypercalciuria. J Clin Invest 47:2580–2590

    Article  PubMed  CAS  Google Scholar 

  21. Weisinger JR, Alonzo E, Bellorin-Font E et al (1996) Possible role of cytokines on the bone mineral loss in idiopathic hypercalciuria. Kidney Int 49:244–250

    Article  PubMed  CAS  Google Scholar 

  22. Ghazali A, Fuentes V, Desaint C et al (1997) Low bone mineral density and peripheral blood monocyte activation profile in calcium stone formers with idiopathic hypercalciuria. J Clin Endocrinol Metab 82:32–38

    Article  PubMed  CAS  Google Scholar 

  23. Steiniche T, Mosekilde L, Christensen MS, Melsen F (1989) Histomorphometric analysis of bone in idiopathic hypercalciuria before and after treatment with thiazide. APMIS 97:302–308

    Article  PubMed  CAS  Google Scholar 

  24. Letavernier E, Traxer O, Daudon M, Tligui M, Hubert-Brierre J, Guerrot D, Sebag A, Baud L, Haymann JP (2011) Determinants of osteopenia in male renal-stone-disease patients with idiopathic hypercalciuria. Clin J Am Soc Nephrol 6:1149–1154

    Article  PubMed  Google Scholar 

  25. Lemann J Jr, Bushinsky DA, Hamm LL (2003) Bone buffering of acid and base in humans. Am J Physiol Renal Physiol 285:F811–F832

    PubMed  CAS  Google Scholar 

  26. Bushinsky DA, Frick KK, Nehrke K (2006) Genetic hypercalciuric stone-forming rats. Curr Opin Nephrol Hypertens 15:403–418

    Article  PubMed  CAS  Google Scholar 

  27. Bushinsky DA, Favus MJ (1988) Mechanism of hypercalciuria in genetic hypercalciuric rats: inherited defect in intestinal calcium transport. J Clin Invest 82:1585–1591

    Article  PubMed  CAS  Google Scholar 

  28. Kim M, Sessler NE, Tembe V, Favus MJ, Bushinsky DA (1993) Response of genetic hypercalciuric rats to a low calcium diet. Kidney Int 43:189–196

    Article  PubMed  CAS  Google Scholar 

  29. Coe FL, Favus MJ, Crockett T, Strauss AL, Parks JH, Porat A, Gantt C, Sherwood LM (1982) Effects of low-calcium diet on urine calcium excretion, parathyroid function and serum 1,25(OH)2D3 levels in patients with idiopathic hypercalciuria and in normal subjects. Am J Med 72:25–32

    Article  PubMed  CAS  Google Scholar 

  30. Pak CY (1998) Kidney stones. Lancet 351:1797–1801

    Article  PubMed  CAS  Google Scholar 

  31. Bushinsky DA, Neumann KJ, Asplin J, Krieger NS (1999) Alendronate decreases urine calcium and supersaturation in genetic hypercalciuric rats. Kidney Int 55:234–243

    Article  PubMed  CAS  Google Scholar 

  32. Krieger NS, Stathopoulos VM, Bushinsky DA (1996) Increased sensitivity to 1,25(OH)2D3 in bone from genetic hypercalciuric rats. Am J Physiol Cell Physiol 271:C130–C135

    CAS  Google Scholar 

  33. Tsuruoka S, Bushinsky DA, Schwartz GJ (1997) Defective renal calcium reabsorption in genetic hypercalciuric rats. Kidney Int 51:1540–1547

    Article  PubMed  CAS  Google Scholar 

  34. Yao J, Karnauskas AJ, Bushinsky DA, Favus MJ (2005) Regulation of renal calcium-sensing receptor gene expression in response to 1,25(OH)2D3 in genetic hypercalciuric stone forming rats. J Am Soc Nephrol 16:1300–1308

    Article  PubMed  CAS  Google Scholar 

  35. Karnauskas AJ, van Leeuwen JP, van den Bemd GJ, Kathpalia PP, DeLuca HF, Bushinsky DA, Favus MJ (2005) Mechanism and function of high vitamin D receptor levels in genetic hypercalciuric stone-forming rats. J Bone Miner Res 20:447–454

    Article  PubMed  CAS  Google Scholar 

  36. Bai S, Wang H, Shen J, Zhou R, Bushinsky DA, Favus MJ (2010) Elevated vitamin D receptor levels in genetic hypercalciuric stone-forming rats are associated with downregulation of Snail. J Bone Miner Res 25:830–840

    PubMed  CAS  Google Scholar 

  37. Li XQ, Tembe V, Horwitz GM, Bushinsky DA, Favus MJ (1993) Increased intestinal vitamin D receptor in genetic hypercalciuric rats: a cause of intestinal calcium hyperabsorption. J Clin Invest 91:661–667

    Article  PubMed  CAS  Google Scholar 

  38. Larriba MJ, Bonilla F, Muñoz A (2010) The transcription factors Snail1 and Snail2 repress vitamin D receptor during colon cancer progression. J Steroid Biochem Mol Biol 121:106–109

    Article  PubMed  CAS  Google Scholar 

  39. Favus MJ, Karnauskas AJ, Parks JH, Coe FL (2004) Peripheral blood monocyte vitamin D receptor levels are elevated in patients with idiopathic hypercalciuria. J Clin Endocrinol Metab 89:4937–4943

    Article  PubMed  CAS  Google Scholar 

  40. Bushinsky DA, Grynpas MD, Nilsson EL, Nakagawa Y, Coe FL (1995) Stone formation in genetic hypercalciuric rats. Kidney Int 48:1705–1713

    Article  PubMed  CAS  Google Scholar 

  41. Asplin JR, Bushinsky DA, Singharetnam W, Riordon D, Parks JH, Coe FL (1997) Relationship between supersaturation and crystal inhibition in hypercalciuric rats. Kidney Int 51:640–645

    Article  PubMed  CAS  Google Scholar 

  42. Bushinsky DA, Parker WR, Asplin JR (2000) Calcium phosphate supersaturation regulates stone formation in genetic hypercalciuric stone-forming rats. Kidney Int 57:550–560

    Article  PubMed  CAS  Google Scholar 

  43. Evan AP, Lingeman JE, Coe FL, Parks JH, Bledsoe SB, Shao Y, Sommer AJ, Paterson RF, Kuo RL, Grynpas M (2003) Randall’s plaque of patients with nephrolithiasis begins in basement membranes of thin loops of Henle. J Clin Invest 111:607–616

    PubMed  CAS  Google Scholar 

  44. Bushinsky DA (2003) Nephrolithiasis: site of the initial solid phase. J Clin Invest 111:602–605

    PubMed  CAS  Google Scholar 

  45. Bushinsky DA, Asplin JR, Grynpas MD, Evan AP, Parker WR, Alexander KM, Coe FL (2002) Calcium oxalate stone formation in genetic hypercalciuric stone-forming rats. Kidney Int 61:975–987

    Article  PubMed  CAS  Google Scholar 

  46. Grynpas M, Waldman S, Holmyard D, Bushinsky DA (2009) Genetic hypercalciuric stone-forming rats have a primary decrease in bone mineral density and strength. J Bone Miner Res 24:1420–1426

    Article  PubMed  CAS  Google Scholar 

  47. Friedman PA, Bushinsky DA (1999) Diuretic effects on calcium metabolism. Semin Nephrol 19:551–556

    PubMed  CAS  Google Scholar 

  48. Coe FL, Parks JH, Bushinsky DA, Langman CB, Favus MJ (1988) Chlorthalidone promotes mineral retention in patients with idiopathic hypercalciuria. Kidney Int 33:1140–1146

    Article  PubMed  CAS  Google Scholar 

  49. Bushinsky DA, Asplin JR (2005) Thiazides reduce brushite, but not calcium oxalate, supersaturation and stone formation in genetic hypercalciuric stone-forming rats. J Am Soc Nephrol 16:417–424

    Article  PubMed  CAS  Google Scholar 

  50. Breslau NA, Moses AM, Weiner IM (1976) The role of volume contraction in the hypocalciuric action of chlorothiazide. Kidney Int 10:164–170

    Article  PubMed  CAS  Google Scholar 

  51. Pearle MS, Roehrborn CG, Pak CYC (1999) Meta-analysis of randomized trials for medical prevention of calcium oxalate nephrolithiasis. J Endourol 13:679–685

    Article  PubMed  CAS  Google Scholar 

  52. Ernst ME, Carter BL, Zheng S, Grimm RH (2010) Meta-analysis of dose–response characteristics of hydrochlorothiazide and chlorthalidone: effects on systolic blood pressure and potassium. Am J Hypertens 23:440–446

    Article  PubMed  CAS  Google Scholar 

  53. Renjmark L, Vestergaard P, Mosekilde L (2005) Reduced fracture risk in users of thiazide diuretics. Calcif Tissue Int 76:167–175

    Article  Google Scholar 

  54. Feskanisch D, Willett WC, Stampfer JM, Golditz GA (1997) A prospective study of thiazide use and fractures in women. Osteoporos Int 7:79–84

    Article  Google Scholar 

  55. Sigurdsson G, Franzson L (2001) Increased bone mineral density in a population-based group of 70-year-old women on thiazide diuretics, independent of parathyroid hormone levels. J Intern Med 250:51–56

    Article  PubMed  CAS  Google Scholar 

  56. Vescini F, Buffa A, La Manna G, Ciavatti A, Rizzoli E, Bottura A, Stefoni S, Caudarella R (2005) Long-term potassium citrate therapy and bone mineral density in idiopathic calcium stone formers. J Endocrinol Invest 28:218–222

    PubMed  CAS  Google Scholar 

  57. Bushinsky DA, Willett T, Asplin JR, Culbertson C, Che SPY, Grynpas M (2011) Chlorthalidone improves vertebral bone quality in genetic hypercalciuric stone-forming rats. J Bone Miner Res 26:1904–1912

    Article  PubMed  CAS  Google Scholar 

  58. Bushinsky DA, Favus MJ, Coe FL (1984) Mechanism of chronic hypocalciuria with chlorthalidone: reduced calcium absorption. Am J Physiol Renal Fluid Electrolyte Physiol 247:F746–F752

    CAS  Google Scholar 

  59. Hall TJ, Schaueblin M (1994) Hydrochlorothiazide inhibits osteoclastic bone resorption in vitro. Calcif Tissue Int 55:266–268

    Article  PubMed  CAS  Google Scholar 

  60. Lalande A, Roux S, Denne MA, Stanley ER, Schiavi P, Guez D, De Vernejoul MC (2001) Indapamide, a thiazide-like diuretic, decreases bone resorption in vitro. J Bone Miner Res 16:361–370

    Article  PubMed  CAS  Google Scholar 

  61. Barry EL, Gesek FA, Kaplan MR, Hebert SC, Friedman PA (1997) Expression of the sodium-chloride cotransporter in osteoblast-like cells: effect of thiazide diuretics. Am J Physiol Cell Physiol 272:C109–C116

    CAS  Google Scholar 

  62. Aubin R, Menard P, Lajeunesse D (1996) Selective effect of thiazides on the human osteoblast-like cell line MG-63. Kidney Int 50:1476–1482

    Article  PubMed  CAS  Google Scholar 

  63. Lajeunesse D, Delalandre A, Guggino SE (2000) Thiazide diuretics affect osteocalcin production in human osteoblasts at the transcription level without affecting vitamin D3 receptors. J Bone Miner Res 15:894–901

    Article  PubMed  CAS  Google Scholar 

  64. Dvorak MM, De Joussineau C, Carter DH, Pisitkun T, Knepper MA, Gamba G, Kemp PJ, Riccardi D (2007) Thiazide diuretics directly induce osteoblast differentiation and mineralized nodule formation by interacting with a sodium chloride co-transporter in bone. J Am Soc Nephrol 18:2509–2516

    Article  PubMed  CAS  Google Scholar 

  65. Stamatelou KK, Francis ME, Jones CA, Nyberg LM, Curhan GC (2003) Time trends in reported prevalence of kidney stones in the United States: 1976–1994. Kidney Int 63:1817–1823

    Article  PubMed  Google Scholar 

  66. Sakhaee K, Maalouf NM, Sinnott B (2012) Clinical review. Kidney stones 2012: pathogenesis, diagnosis, and management. J Clin Endocrinol Metab 97:1847–1860

    Article  PubMed  CAS  Google Scholar 

  67. Sakhaee K, Maalouf NM, Kumar R, Pasch A, Moe OW (2011) Nephrolithiasis-associated bone disease: pathogenesis and treatment options. Kidney Int 79:393–403

    Article  PubMed  CAS  Google Scholar 

  68. Trombetti A, Herrmann F, Hoffmeyer P, Schurch MA, Bonjour JP, Rizzoli R (2002) Survival and potential years of life lost after hip fracture in men and age-matched women. Osteoporos Int 13:731–737

    Article  PubMed  CAS  Google Scholar 

  69. Asplin JR, Donahue SE, Lindeman C, Michalenka A, Strutz KL, Bushinsky DA (2009) Thiosulfate reduces calcium phosphate nephrolithiasis. J Am Soc Nephrol 20:1246–1253

    Article  PubMed  CAS  Google Scholar 

  70. Hoopes RR, Reid R, Sen S, Szpirer C, Dixon P, Pannet A, Thakker RV, Bushinsky DA, Scheinman SJ (2003) Quantitative trait loci for hypercalciuria in a rat model of kidney stone disease. J Am Soc Nephrol 14:1844–1850

    Article  PubMed  CAS  Google Scholar 

  71. Bushinsky DA, Kim M, Sessler NE, Nakagawa Y, Coe FL (1994) Increased urinary saturation and kidney calcium content in genetic hypercalciuric rats. Kidney Int 45:58–65

    Article  PubMed  CAS  Google Scholar 

  72. Bushinsky DA, LaPlante K, Asplin JR (2006) Effect of cinacalcet on urine calcium excretion and supersaturation in genetic hypercalciuric stone-forming rats. Kidney Int 69:1586–1592

    Article  PubMed  CAS  Google Scholar 

  73. Coe FL, Favus MJ, Asplin JR (2004) Nephrolithiasis. In: Brenner BM, Rector FC Jr (eds) The kidney. WB Saunders, Philadelphia, pp 1819–1866

    Google Scholar 

  74. Yao J, Kathpalia P, Bushinsky DA, Favus MJ (1998) Hyperresponsiveness of vitamin D receptor gene expression to 1,25-dihydroxyvitamin D3: a new characteristic of genetic hypercalciuric stone-forming rats. J Clin Invest 101:2223–2232

    Article  PubMed  CAS  Google Scholar 

  75. Pak CYC, Kaplan R, Bone H (1975) A simple test for the diagnosis of absorptive, resorptive and renal hypercalciurias. N Engl J Med 292:497

    Article  PubMed  CAS  Google Scholar 

  76. Pak CYC, Britton F, Peterson R, Ward D, Northcutt C, Breslau NA, McGuire J, Sakhaee K, Bush S, Nicar M, Norman D, Peters P (1980) Ambulatory evaluation of nephrolithiasis: classification, clinical presentation and diagnostic criteria. Am J Med 69:19–30

    Article  PubMed  CAS  Google Scholar 

  77. Bataille P, Achard JM, Fournier A, Boudailliez B, Westell PF, Esper NE, Bergot C, Jans I, Lalau JD, Petit J, Henon G, Jeantet MAL, Bouillon R, Sebert JL (1991) Diet, vitamin D and vertebral mineral density in hypercalciuric calcium stone formers. Kidney Int 39:1193–1205

    Article  PubMed  CAS  Google Scholar 

  78. Shen FH, Baylink DJ, Nielsen RL, Sherrard DJ, Ivey JL, Haussler MR (1977) Increased serum 1,25-dihydroxyvitamin D in idiopathic hypercalciuria. J Lab Clin Med 90:955–962

    PubMed  CAS  Google Scholar 

  79. Coe FL, Canterbury JM, Firpo JJ, Reiss E (1973) Evidence for secondary hyperparathyroidism in idiopathic hypercalciuria. J Clin Invest 52:134–142

    Article  PubMed  CAS  Google Scholar 

  80. Burckhardt P, Jaeger P (1981) Secondary hyperparathyroidism in idiopathic renal hypercalciuria: fact or theory? J Clin Endocrinol Metab 55:550

    Article  Google Scholar 

  81. Kaplan RA, Haussler MR, Deftos LJ, Bone H, Pak CYC (1977) The role of 1,25 dihydroxyvitamin D in the mediation of intestinal hyperabsorption of calcium in primary hyperparathyroidism and absorptive hypercalciuria. J Clin Invest 59:756–760

    Article  PubMed  CAS  Google Scholar 

  82. Insogna KL, Broadus AE, Dryer BE, Ellison AF, Gertner JM (1985) Elevated production rate of 1,25-dihydroxyvitamin D in patients with absorptive hypercalciuria. J Clin Endocrinol Metab 61:490–495

    Article  PubMed  CAS  Google Scholar 

  83. Zerwekh JE, Reed BY, Heller HJ, Gonzalez GB, Haussler MR, Pak CY (1998) Normal vitamin D receptor concentration and responsiveness to 1,25-dihydroxyvitamin D3 in skin fibroblasts from patients with absorptive hypercalciuria. Miner Electrolyte Metab 24:307–313

    Article  PubMed  CAS  Google Scholar 

  84. Rendina D, Mossetti G, Viceconti R, Sorrentino M, Castaldo R, Manno G, Guadagno V, Strazzullo P, Nunziata V (2004) Association between vitamin D receptor gene polymorphisms and fasting idiopathic hypercalciuria in recurrent stone-forming patients. Urology 64:833–838

    Article  PubMed  Google Scholar 

  85. Bid HK, Kumar A, Kapoor R, Mittal RD (2005) Association of vitamin D receptor gene (Fokl) polymorphism with calcium oxalate nephrolithiasis. J Endourol 19:111–115

    Article  PubMed  Google Scholar 

  86. Chen WC, Chen HY, Lu HF, Hsu CD, Tsai FJ (2001) Association of the vitamin D receptor gene start codon Fok I polymorphism with calcium oxalate stone disease. BJU Int 87:168–171

    Article  PubMed  CAS  Google Scholar 

  87. Valdivielso JM, Fernandez E (2006) Vitamin D receptor polymorphisms and diseases. Clin Chim Acta 371:1–12

    Article  PubMed  CAS  Google Scholar 

  88. Jackman SV, Kibel AS, Ovuworie CA, Moore RG, Kavoussi LR, Jarrett TW (1999) Familial calcium stone disease: Taql polymorphism and the vitamin D receptor. J Endourol 13:313–316

    Article  PubMed  CAS  Google Scholar 

  89. Favus MJ (1994) Hypercalciuria: lessons from studies of genetic hypercalciuric rats. J Am Soc Nephrol 5:S54–S58

    PubMed  CAS  Google Scholar 

  90. Gambaro G, Vezzoli G, Casari G, Rampoldi L, D’Angelo A, Borghi L (2004) Genetics of hypercalciuria and calcium nephrolithiasis: from the rare monogenic to the common polygenic forms. Am J Kidney Dis 44:963–986

    Article  PubMed  CAS  Google Scholar 

  91. Chattopadhyay N, Brown EM (2006) Role of calcium-sensing receptor in mineral ion metabolism and inherited disorders of calcium-sensing. Mol Genet Metab 89:189–202

    Article  PubMed  CAS  Google Scholar 

  92. Vezzoli G, Tanini A, Ferrucci L, Soldati L, Bianchin C, Franceschelli F, Malentacchi C, Porfirio B, Adamo D, Terranegra A, Falchetti A, Cusi D, Bianchi G, Brandi ML (2002) Influence of calcium-sensing receptor gene on urinary calcium excretion in stone-forming patients. J Am Soc Nephrol 13:2517–2523

    Article  PubMed  CAS  Google Scholar 

  93. Scillitani A, Guarnieri V, De Geronimo S, Muscarella LA, Battista C, D’Agruma L, Bertoldo F, Florio C, Minisola S, Hendy GN, Cole DEC (2004) Blood ionized calcium is associated with clustered polymorphisms in the carboxyl-terminal tail of the calcium-sensing receptor. J Clin Endocrinol Metab 89:5634–5638

    Article  PubMed  CAS  Google Scholar 

  94. Parks JH, Coe FL (1996) Pathogenesis and treatment of calcium stones. Semin Nephrol 16:398–411

    PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by Grants RO1 DK 75462 and AR 46289 from the National Institutes of Health.

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  1. Division of Nephrology, Department of Medicine, University of Rochester School of Medicine, 601 Elmwood Ave., Box 675, Rochester, NY, 14642, USA

    Nancy S. Krieger & David A. Bushinsky

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  1. Nancy S. Krieger
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Correspondence to Nancy S. Krieger.

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Krieger, N.S., Bushinsky, D.A. The Relation Between Bone and Stone Formation. Calcif Tissue Int 93, 374–381 (2013). https://doi.org/10.1007/s00223-012-9686-2

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