Abstract
Deposition of calcium oxalate crystals in the kidney and bone is a hallmark of primary hyperoxaluria (PH). Since the bone compartment can store massive amounts of oxalate, patients present with recurrent low-trauma fractures, bone deformations, severe bone pains, and specific oxalate osteopathy on X-ray. Bone biopsy from the iliac crest displays specific features such as oxalate crystals surrounded by a granulomatous reaction corresponding to an invasion of bone surface by macrophages. The objective of this manuscript is therefore to provide an overview of bone impairment in PH, by reviewing the current literature on bone and dental symptoms as well as imaging techniques used for assessing bone disease.
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References
Marengo SR, Romani AM (2008) Oxalate in renal stone disease: the terminal metabolite that just won’t go away. Nat Clin Pract Nephrol 4:368–377
Cochat P, Rumsby G (2013) Primary hyperoxaluria. N Engl J Med 369:649–658
Cochat P, Liutkus A, Fargue S, Basmaison O, Ranchin B, Rolland MO (2006) Primary hyperoxaluria type 1: still challenging! Pediatr Nephrol 21:1075–1081
Belostotsky R, Seboun E, Idelson GH, Milliner DS, Becker-Cohen R, Rinat C, Monico CG, Feinstein S, Ben-Shalom E, Magen D, Weissman I, Charon C, Frishberg Y (2010) Mutations in DHDPSL are responsible for primary hyperoxaluria type III. Am J Hum Genet 87:392–399
Marangella M, Vitale C, Petrarulo M, Tricerri A, Cerelli E, Cadario A, Barbos MP, Linari F (1995) Bony content of oxalate in patients with primary hyperoxaluria or oxalosis-unrelated renal failure. Kidney Int 48:182–187
Toussaint C, Vienne A, De Pauw L, Gelin M, Janssen F, Hall M, Schurmans T, Pasteels JL (1995) Combined liver-kidney transplantation in primary hyperoxaluria type 1. Bone histopathology and oxalate body content. Transplantation 59:1700–1704
Morgan SH, Purkiss P, Watts RW, Mansell MA (1987) Oxalate dynamics in chronic renal failure. Comparison with normal subjects and patients with primary hyperoxaluria. Nephron 46:253–257
Marangella M, Cosseddu D, Petrarulo M, Vitale C, Linari F (1993) Thresholds of serum calcium oxalate supersaturation in relation to renal function in patients with or without primary hyperoxaluria. Nephrol Dial Transplant 8:1333–1337
Bacchetta J, Harambat J, Cochat P, Salusky IB, Wesseling-Perry K (2012) The consequences of chronic kidney disease on bone metabolism and growth in children. Nephrol Dial Transplant 27:3063–3071
El Hage S, Ghanem I, Baradhi A, Mourani C, Mallat S, Dagher F, Kharrat K (2008) Skeletal features of primary hyperoxaluria type 1, revisited. J Child Orthop 2:205–210
Harambat J, van Stralen KJ, Espinosa L, Groothoff JW, Hulton SA, Cerkauskiene R, Schaefer F, Verrina E, Jager KJ, Cochat P, European Society for Pediatric Nephrology/European Renal Association-European Dialysis and Transplant Association (ESPN/ERA-EDTA) Registry (2012) Characteristics and outcomes of children with primary oxalosis requiring renal replacement therapy. Clin J Am Soc Nephrol 7:458–465
Nissel R, Latta K, Gagnadoux MF, Kelly D, Hulton S, Kemper MJ, Ruder H, Soderdahl G, Otte JB, Cochat P, Roquet O, Jamieson NV, Haffner D (2006) Body growth after combined liver-kidney transplantation in children with primary hyperoxaluria type 1. Transplantation 82:48–54
Tammachote R, Kingsuwannapong N, Tongkobpetch S, Srichomthong C, Yeetong P, Kingwatanakul P, Monico CG, Suphapeetiporn K, Shotelersuk V (2012) Primary hyperoxaluria type 1 and brachydactyly mental retardation syndrome caused by a novel mutation in AGXT and a terminal deletion of chromosome 2. Am J Med Genet A 158A:2124–2130
Verbruggen LA, Bourgain C, Verbeelen D (1989) Late presentation and microcrystalline arthropathy in primary hyperoxaluria. Clin Exp Rheumatol 7:631–633
Bernhardt WM, Schefold JC, Weichert W, Rudolph B, Frei U, Groneberg DA, Schindler R (2006) Amelioration of anemia after kidney transplantation in severe secondary oxalosis. Clin Nephrol 65:216–221
Salido EC, Li XM, Lu Y, Wang X, Santana A, Roy-Chowdhury N, Torres A, Shapiro LJ, Roy-Chowdhury J (2006) Alanine-glyoxylate aminotransferase-deficient mice, a model for primary hyperoxaluria that responds to adenoviral gene transfer. Proc Natl Acad Sci U S A 103:18249–18254
Day DL, Scheinman JI, Mahan J (1986) Radiological aspects of primary hyperoxaluria. Am J Roentgenol 146:395–401
Brancaccio D, Poggi A, Ciccarelli C, Bellini F, Galmozzi C, Poletti I, Maggiore Q (1981) Bone changes in end-stage oxalosis. Am J Roentgenol 136:935–939
Kamoun A, Hammou A, Chaouachi S, Bellagha I, Lakhoua R (1995) Radiological signs of type I primary hyperoxaluria. Ann Radiol (Paris) 38:440–446
Wiggelinkhuizen J, Fisher RM (1982) Oxalosis of bone. Pediatr Radiol 12:307–309
Fisher D, Hiller N, Drukker A (1995) Oxalosis of bone: report of four cases and a new radiological staging. Pediatr Radiol 25:293–295
Ring E, Wendler H, Ratschek M, Zobel G (1989) Bone disease of primary hyperoxaluria in infancy. Pediatr Radiol 20:131–133
Bacchetta J, Fargue S, Boutroy S, Basmaison O, Vilayphiou N, Plotton I, Guebre-Egziabher F, Dohin B, Kohler R, Cochat P (2010) Bone metabolism in oxalosis: a single-center study using new imaging techniques and biomarkers. Pediatr Nephrol 25:1081–1089
Orazi C, Picca S, Schingo PM, Fassari FM, Canepa G (2009) Oxalosis in primary hyperoxaluria in infancy: Report of a case in a 3-month-old baby. Follow-up for 3 years and review of literature. Skeletal Radiol 38:387–391
Behnke B, Kemper MJ, Kruse HP, Muller-Wiefel DE (2001) Bone mineral density in children with primary hyperoxaluria type I. Nephrol Dial Transplant 16:2236–2239
Stenger KO, Sterneck M, Kromminga A (2014) TRACP5b als ein alternativer marker für schwere und fortschreiten der erkrankung an prïmarer hyperoxalurie typ 1. Nieren und Hochdruckkrankheiten:217–228
Glass RT (1973) Oral manifestations in primary hyperoxaluria and oxalosis. Report of a case. Oral Surg Oral Med Oral Pathol 35:502–509
Mitsimponas KT, Wehrhan T, Falk S, Wehrhan F, Neukam FW, Schlegel KA (2012) Oral findings associated with primary hyperoxaluria type I. J Craniomaxillofac Surg 40:e301–e306
Moskow BS (1989) Periodontal manifestations of hyperoxaluria and oxalosis. J Periodontol 60:271–278
Guerra EN, Vianna L, Sobreira MN, de Araujo FN, de Melo NS (2011) Oral manifestations of hyperoxaluria. J Craniofac Surg 22:2191–2192
Hernandez JD, Wesseling K, Pereira R, Gales B, Harrison R, Salusky IB (2008) Technical approach to iliac crest biopsy. Clin J Am Soc Nephrol 3(Suppl 3):S164–S169
Benhamou CL, Pierre D, Geslin N, Viala JF, Maitre F, Chavassieux P, Edouard C, Meunier PJ (1987) Primary bone oxalosis: the roles of oxalate deposits and renal osteodystrophy. Bone 8:59–64
Adams ND, Carrera GF, Johnson RP, Latorraca R, Lemann J Jr (1982) Calcium-oxalate-crystal-induced bone disease. Am J Kidney Dis 1:294–299
Milgram JW, Salyer WR (1974) Secondary oxalosis of bone in chronic renal failure. A histopathological study of three cases. J Bone Joint Surg Am 56:387–395
Brady HR, Fay WP, Meema HE, Rabinovich S, Rapoport A, Oreopoulos DG (1989) Oxalate bone disease–an emerging form of renal osteodystrophy. Int J Artif Organs 12:715–719
Benhamou CL, Bardin T, Tourliere D, Voisin L, Audran M, Edouard C, Lafage MH, Sebert JL, de Vernejoul MC, Wendling D (1991) Bone involvement in primary oxalosis. Study of 20 cases. Rev Rhum Mal Osteoartic 58:763–769
Bala Y, Farlay D, Boivin G (2013) Bone mineralization: from tissue to crystal in normal and pathological contexts. Osteoporos Int 24:2153–2166
Gherardi G, Poggi A, Sisca S, Calderaro V, Bonucci E (1980) Bone oxalosis and renal osteodystrophy. Arch Pathol Lab Med 104:105–111
Jahn H, Frank RM, Voegel JC, Schohn D (1980) Scanning electron microscopy and x-ray diffraction studies of human bone oxalosis. Calcif Tissue Int 30:109–119
Lagier R, Revell P, Schoenboerner A (1982) Calcium oxalate deposition in growing bone: anatomical and radiological study in a case of primary oxalosis. Metab Bone Dis Relat Res 4:49–59
Cochat P, Hulton SA, Acquaviva C, Danpure CJ, Daudon M, De Marchi M, Fargue S, Groothoff J, Harambat J, Hoppe B, Jamieson NV, Kemper MJ, Mandrile G, Marangella M, Picca S, Rumsby G, Salido E, Straub M, van Woerden CS, OxalEurope (2012) Primary hyperoxaluria Type 1: indications for screening and guidance for diagnosis and treatment. Nephrol Dial Transplant 27:1729–1736
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Bacchetta, J., Boivin, G. & Cochat, P. Bone impairment in primary hyperoxaluria: a review. Pediatr Nephrol 31, 1–6 (2016). https://doi.org/10.1007/s00467-015-3048-z
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DOI: https://doi.org/10.1007/s00467-015-3048-z