Pediatric Nephrology

, Volume 27, Issue 7, pp 1139–1148 | Cite as

Assessment of dual-energy x-ray absorptiometry measures of bone health in pediatric chronic kidney disease

  • Lindsay M. Griffin
  • Heidi J. Kalkwarf
  • Babette S. Zemel
  • Justine Shults
  • Rachel J. Wetzsteon
  • C. Frederic Strife
  • Mary B. Leonard
Original Article



Dual-energy X-ray absorptiometry (DXA) techniques are limited in childhood chronic kidney disease (CKD) by the confounding effect of short stature and opposing parathyroid hormone effects on trabecular and cortical bone. Peripheral quantitative computed tomography (pQCT) is not subject to these limitations.


Lumbar spine (LS) and whole-body (WB) DXA and tibia pQCT scans were obtained in 88 stage 4–5 CKD and >650 healthy participants, ages 5–21 years. Sex- and race-specific Z-scores were generated for bone mineral density (BMD) and bone mineral content (BMC) by DXA, relative to age and adjusted for height Z-score (LS-BMD-Z and WB-BMC-Z), and compared to pQCT Z-scores for trabecular BMD (TrabBMD-Z) for age and cortical BMC (CortBMC-Z) for age and tibia length.


LS-BMD-Z [0.50 (95% C.I. 0.28, 0.73), p < 0.0001] and TrabBMD-Z [0.53 (0.27, 0.79), p < 0.0001] were greater in CKD, and WB-BMC-Z [–0.36 (–0.53, –0.19), p < 0.0001] and CortBMC-Z [–0.48 (–0.70, –0.27), p < 0.0001] were lower, compared to reference participants. Z-scores were correlated at trabecular (LS-BMD-Z and TrabBMD-Z: R = 0.36) and cortical (WB-BMC-Z and CortBMC-Z: R = 0.64) sites in CKD; similar to correlations in reference participants.


Lumbar spine and whole-body DXA suggested greater trabecular BMD and lower cortical BMC in CKD, consistent with pQCT results; however, correlations were modest. Studies are needed to identify methods that predict fracture in childhood CKD.


Pediatrics Bone Dual-energy X-ray absorptiometry Peripheral quantitative computed tomography Chronic kidney disease 


Funding Sources

NIH R01-DK060030, R01-HD040714, K24-DK076808, and UL1-RR-024134


  1. 1.
    NIH Osteoporosis Prevention, Diagnosis, and Therapy (2000) NIH Consensus Statement 17(1):1–36Google Scholar
  2. 2.
    Cunningham J, Sprague SM, Cannata-Andia J, Coco M, Cohen-Solal M, Fitzpatrick L, Goltzmann D, Lafage-Proust MH, Leonard M, Ott S, Rodriguez M, Stehman-Breen C, Stern P, Weisinger J (2004) Osteoporosis in chronic kidney disease. Am J Kidney Dis 43(3):566–571PubMedCrossRefGoogle Scholar
  3. 3.
    Bishop N, Braillon P, Burnham J, Cimaz R, Davies J, Fewtrell M, Hogler W, Kennedy K, Makitie O, Mughal Z, Shaw N, Vogiatzi M, Ward K, Bianchi ML (2008) Dual-energy X-ray absorptiometry assessment in children and adolescents with diseases that may affect the skeleton: the 2007 ISCD Pediatric Official Positions. J Clin Densitom 11(1):29–42PubMedCrossRefGoogle Scholar
  4. 4.
    Parfitt AM (1998) A structural approach to renal bone disease. J Bone Miner Res 13(8):1213–1220PubMedCrossRefGoogle Scholar
  5. 5.
    Prentice A, Parsons TJ, Cole TJ (1994) Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants. Am J Clin Nutr 60(6):837–842PubMedGoogle Scholar
  6. 6.
    Saland JM, Goode ML, Haas DL, Romano TA, Seikaly MG (2001) The prevalence of osteopenia in pediatric renal allograft recipients varies with the method of analysis. Am J Transplant 1(3):243–250PubMedCrossRefGoogle Scholar
  7. 7.
    Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, Mahboubi S, Shepherd JA, Hangartner TN, Frederick MM, Winer KK, Kalkwarf HJ (2010) Height adjustment in assessing dual-energy X-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 95(3):1265–1273PubMedCrossRefGoogle Scholar
  8. 8.
    Wetzsteon RJ, Kalkwarf HJ, Shults J, Zemel BS, Foster BJ, Griffin L, Strife CF, Foerster DL, Jean-Pierre DK, Leonard MB (2011) Volumetric bone mineral density and bone structure in childhood chronic kidney disease. J Bone Miner Res 26(9):2235–44PubMedCrossRefGoogle Scholar
  9. 9.
    Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, Frederick MM, Huang X, Lu M, Mahboubi S, Hangartner T, Winer KK (2011) Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the Bone Mineral Density in Childhood Study. J Clin Endocrinol Metab 96:3160–3169PubMedCrossRefGoogle Scholar
  10. 10.
    Tuchman S, Kalkwarf HJ, Zemel BS, Shults J, Wetzsteon RJ, Foerster D, Strife CF, Leonard MB (2010) Vitamin D deficiency and parathyroid hormone levels following renal transplantation in children and adolescents. Pediatr Nephrol 25(12):2509–2516PubMedCrossRefGoogle Scholar
  11. 11.
    Foster BJ, Kalkwarf HJ, Shults J, Zemel BS, Wetzsteon RJ, Thayu M, Foerster DL, Leonard MB (2011) Association of chronic kidney disease with muscle deficits in children. J Am Soc Nephrol 22(2):377–386PubMedCrossRefGoogle Scholar
  12. 12.
    Tanner JM (1962) Growth at adolescence, 2nd edn. Blackwell Scientific Publications, OxfordGoogle Scholar
  13. 13.
    Tanner JM, Whitehouse RH, Marshall WA, Healy MJR, Goldstein H (1975) Assessment of skeletal maturity and prediction of adult height (TW2 method). Academic Press, LondonGoogle Scholar
  14. 14.
    Gordon CM, Bachrach LK, Carpenter TO, Crabtree N, El-Hajj Fuleihan G, Kutilek S, Lorenc RS, Tosi LL, Ward KA, Ward LM, Kalkwarf HJ (2008) Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the 2007 ISCD Pediatric Official Positions. J Clin Densitom 11:43–58PubMedCrossRefGoogle Scholar
  15. 15.
    Shepherd JA, Wang L, Fan B, Gilsanz V, Kalkwarf HJ, Lappe J, Lu Y, Hangartner T, Zemel BS, Frederick M, Oberfield S, Winer KK (2011) Optimal monitoring time interval between DXA measures in children. J Bone Miner Res 26(11):2745–2752PubMedCrossRefGoogle Scholar
  16. 16.
    Schwartz GJ, Munoz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20(3):629–637PubMedCrossRefGoogle Scholar
  17. 17.
    Gao P, Scheibel S, D'Amour P, John MR, Rao SD, Schmidt-Gayk H, Cantor TL (2001) Development of a novel immunoradiometric assay exclusively for biologically active whole parathyroid hormone 1-84: implications for improvement of accurate assessment of parathyroid function. J Bone Miner Res 16(4):605–614PubMedCrossRefGoogle Scholar
  18. 18.
    Ogden CL, Kuczmarski RJ, Flegal KM, Mei Z, Guo S, Wei R, Grummer-Strawn LM, Curtin LR, Roche AF, Johnson CL (2002) Centers for Disease Control and Prevention 2000 growth charts for the United States: improvements to the 1977 National Center for Health Statistics version. Pediatrics 109(1):45–60PubMedCrossRefGoogle Scholar
  19. 19.
    Dubner SE, Shults J, Baldassano RN, Zemel BS, Thayu M, Burnham JM, Herskovitz RM, Howard KM, Leonard MB (2009) Longitudinal assessment of bone density and structure in an incident cohort of children with Crohn's disease. Gastroenterology 136(1):123–130PubMedCrossRefGoogle Scholar
  20. 20.
    Wetzsteon RJ, Shults J, Zemel BS, Gupta PU, Burnham JM, Herskovitz RM, Howard KM, Leonard MB (2009) Divergent effects of glucocorticoids on cortical and trabecular compartment BMD in childhood nephrotic syndrome. J Bone Miner Res 24(3):503–513PubMedCrossRefGoogle Scholar
  21. 21.
    Cole TJ (1990) The LMS method for constructing normalized growth standards. Eur J Clin Nutr 44(1):45–60PubMedGoogle Scholar
  22. 22.
    Kelly TL, Wilson KE, Heymsfield SB (2009) Dual-energy X-ray absorptiometry body composition reference values from NHANES. PLoS One 4(9):e7038PubMedCrossRefGoogle Scholar
  23. 23.
    Sanchez CP, Salusky IB, Kuizon BD, Ramirez JA, Gales B, Ettenger RB, Goodman WG (1998) Bone disease in children and adolescents undergoing successful renal transplantation. Kidney Int 53(5):1358–1364PubMedCrossRefGoogle Scholar
  24. 24.
    Reusz GS, Szabo AJ, Peter F, Kenesei E, Sallay P, Latta K, Szabo A, Tulassay T (2000) Bone metabolism and mineral density following renal transplantation. Arch Dis Child 83(2):146–151PubMedCrossRefGoogle Scholar
  25. 25.
    Ahmed SF, Russell S, Rashid R, Beattie TJ, Murphy AV, Ramage IJ, Maxwell H (2005) Bone mineral content, corrected for height or bone area, measured by DXA is not reduced in children with chronic renal disease or in hypoparathyroidism. Pediatr Nephrol 20(10):1466–1472PubMedCrossRefGoogle Scholar
  26. 26.
    KDOQI Clinical Practice Guidelines for bone metabolism and disease in children with chronic kidney disease (2005) Am J of Kid Diseases 46(1):S1–S103Google Scholar
  27. 27.
    KDIGO Clinical Practice Guideline for the Diagnosis, Evaluation, Prevention, and Treatment of Chronic Kidney Disease-Mineral and Bone Disorder (CKD-MBD) (2009) Kidney Int 76(113):S1Google Scholar
  28. 28.
    Andrade MC, Carvalhaes JT, Carvalho AB, Lazarretti-Castro M, Brandao C (2007) Bone mineral density and bone histomorphometry in children on long-term dialysis. Pediatr Nephrol 22(10):1767–1772PubMedCrossRefGoogle Scholar
  29. 29.
    Pluskiewicz W, Adamczyk P, Drozdzowska B, Szprynger K, Szczepanska M, Halaba Z, Karasek D (2002) Skeletal status in children, adolescents and young adults with end-stage renal failure treated with hemo- or peritoneal dialysis. Osteoporos Int 13(5):353–357PubMedCrossRefGoogle Scholar
  30. 30.
    Pluskiewicz W, Adamczyk P, Drozdzowska B, Szprynger K, Szczepanska M, Halaba Z, Karasek D (2003) Skeletal status in children and adolescents with chronic renal failure before onset of dialysis or on dialysis. Osteoporos Int 14(4):283–288PubMedCrossRefGoogle Scholar
  31. 31.
    Pluskiewicz W, Adamczyk P, Drozdzowska B, Szprynger K, Szczepanska M, Halaba Z, Karasek D (2005) Skeletal status in adolescents with end-stage renal failure: a longitudinal study. Osteoporos Int 16(3):289–295PubMedCrossRefGoogle Scholar
  32. 32.
    Bakr AM (2004) Bone mineral density and bone turnover markers in children with chronic renal failure. Pediatr Nephrol 19(12):1390–1393PubMedCrossRefGoogle Scholar
  33. 33.
    Waller S, Ridout D, Rees L (2007) Bone mineral density in children with chronic renal failure. Pediatr Nephrol 22(1):121–127PubMedCrossRefGoogle Scholar
  34. 34.
    Van Dyck M, Gyssels A, Proesmans W, Nijs J, Eeckels R (2001) Growth hormone treatment enhances bone mineralisation in children with chronic renal failure. Eur J Pediatr 160(6):359–363PubMedCrossRefGoogle Scholar
  35. 35.
    van der Sluis IM, Boot AM, Nauta J, Hop WC, de Jong MC, Lilien MR, Groothoff JW, van Wijk AE, Pols HA, Hokken-Koelega AC, de Muinck Keizer-Schrama SM (2000) Bone density and body composition in chronic renal failure: effects of growth hormone treatment. Pediatr Nephrol 15(3–4):221–228PubMedCrossRefGoogle Scholar
  36. 36.
    Swolin-Eide D, Magnusson P, Hansson S (2007) Bone mass, biochemical markers and growth in children with chronic kidney disease: a 1-year prospective study. Acta Paediatr 96(5):720–725PubMedCrossRefGoogle Scholar
  37. 37.
    Swolin-Eide D, Hansson S, Magnusson P (2009) Children with chronic kidney disease: a 3-year prospective study of growth, bone mass and bone turnover. Acta Paediatr 98(2):367–373PubMedCrossRefGoogle Scholar
  38. 38.
    Behnke B, Altrogge H, Delling G, Kruse HP, Muller-Wiefel DE (1996) Bone mineral density in pediatric patients after renal transplantation. Clin Nephrol 46(1):24–29PubMedGoogle Scholar
  39. 39.
    Behnke B, Kemper MJ, Kruse HP, Muller-Wiefel DE (2001) Bone mineral density in children with primary hyperoxaluria type I. Nephrol Dial Transplant 16(11):2236–2239PubMedCrossRefGoogle Scholar
  40. 40.
    Lima EM, Goodman WG, Kuizon BD, Gales B, Emerick A, Goldin J, Salusky IB (2003) Bone density measurements in pediatric patients with renal osteodystrophy. Pediatr Nephrol 18(6):554–559PubMedGoogle Scholar
  41. 41.
    Mehls O, Ritz E, Krempien B, Willich E, Bommer J, Scharer K (1973) Roentgenological signs in the skeleton of uremic children. An analysis of the anatomical principles underlying the roentgenological changes. Pediatr Radiol 1(3):183–190PubMedCrossRefGoogle Scholar
  42. 42.
    Sanchez CP, He YZ (2003) Effects of thyroparathyroidectomy, exogenous calcium, and short-term calcitriol therapy on the growth plate in renal failure. J Am Soc Nephrol 14(1):148–158PubMedCrossRefGoogle Scholar
  43. 43.
    Sanchez CP, He YZ, Leiferman E, Wilsman NJ (2004) Bone elongation in rats with renal failure and mild or advanced secondary hyperparathyroidism. Kidney Int 65(5):1740–1748PubMedCrossRefGoogle Scholar
  44. 44.
    Leonard MB, Shults J, Zemel BS (2006) DXA estimates of vertebral volumetric bone mineral density in children: potential advantages of paired posteroanterior and lateral scans. J Clin Densitom 9(3):265–273PubMedCrossRefGoogle Scholar
  45. 45.
    Wren TA, Liu X, Pitukcheewanont P, Gilsanz V (2005) Bone densitometry in pediatric populations: discrepancies in the diagnosis of osteoporosis by DXA and CT. J Pediatr 146(6):776–779PubMedCrossRefGoogle Scholar

Copyright information

© IPNA 2012

Authors and Affiliations

  • Lindsay M. Griffin
    • 1
  • Heidi J. Kalkwarf
    • 2
  • Babette S. Zemel
    • 1
  • Justine Shults
    • 3
  • Rachel J. Wetzsteon
    • 1
  • C. Frederic Strife
    • 2
  • Mary B. Leonard
    • 1
    • 3
  1. 1.Department of PediatricsChildren’s Hospital of PhiladelphiaPhiladelphiaUSA
  2. 2.Department of PediatricsCincinnati Children’s Hospital Medical CenterCincinnatiUSA
  3. 3.Department of Biostatistics and EpidemiologyPerelman School of Medicine at the University of PennsylvaniaPhiladelphiaUSA

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