Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Pediatric Nephrology Aims and scope Submit manuscript

Abstract

Background

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.

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Article Open access 01 July 2023

Enisa Shevroja, Jean-Yves Reginster, … Nicholas C. Harvey

References

  1. NIH Osteoporosis Prevention, Diagnosis, and Therapy (2000) NIH Consensus Statement 17(1):1–36

    Google Scholar 

  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):566–571

    Article  PubMed  Google Scholar 

  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):29–42

    Article  PubMed  Google Scholar 

  4. Parfitt AM (1998) A structural approach to renal bone disease. J Bone Miner Res 13(8):1213–1220

    Article  PubMed  CAS  Google Scholar 

  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):837–842

    PubMed  CAS  Google Scholar 

  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):243–250

    Article  PubMed  CAS  Google Scholar 

  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):1265–1273

    Article  PubMed  CAS  Google Scholar 

  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):2235–44

    Article  PubMed  Google Scholar 

  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 96:3160–3169

    Article  PubMed  CAS  Google Scholar 

  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):2509–2516

    Article  PubMed  Google Scholar 

  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):377–386

    Article  PubMed  Google Scholar 

  12. Tanner JM (1962) Growth at adolescence, 2nd edn. Blackwell Scientific Publications, Oxford

    Google Scholar 

  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, London

    Google Scholar 

  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 11:43–58

    Article  PubMed  Google Scholar 

  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):2745–2752

    Article  PubMed  Google Scholar 

  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):629–637

    Article  PubMed  Google Scholar 

  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):605–614

    Article  PubMed  CAS  Google Scholar 

  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):45–60

    Article  PubMed  Google Scholar 

  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):123–130

    Article  PubMed  Google Scholar 

  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):503–513

    Article  PubMed  CAS  Google Scholar 

  21. Cole TJ (1990) The LMS method for constructing normalized growth standards. Eur J Clin Nutr 44(1):45–60

    PubMed  CAS  Google Scholar 

  22. Kelly TL, Wilson KE, Heymsfield SB (2009) Dual-energy X-ray absorptiometry body composition reference values from NHANES. PLoS One 4(9):e7038

    Article  PubMed  Google Scholar 

  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):1358–1364

    Article  PubMed  CAS  Google Scholar 

  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):146–151

    Article  PubMed  CAS  Google Scholar 

  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):1466–1472

    Article  PubMed  Google Scholar 

  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–S103

    Google Scholar 

  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):S1

    Google Scholar 

  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):1767–1772

    Article  PubMed  Google Scholar 

  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):353–357

    Article  PubMed  CAS  Google Scholar 

  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):283–288

    Article  PubMed  CAS  Google Scholar 

  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):289–295

    Article  PubMed  Google Scholar 

  32. Bakr AM (2004) Bone mineral density and bone turnover markers in children with chronic renal failure. Pediatr Nephrol 19(12):1390–1393

    Article  PubMed  Google Scholar 

  33. Waller S, Ridout D, Rees L (2007) Bone mineral density in children with chronic renal failure. Pediatr Nephrol 22(1):121–127

    Article  PubMed  Google Scholar 

  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):359–363

    Article  PubMed  Google Scholar 

  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):221–228

    Article  PubMed  Google Scholar 

  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):720–725

    Article  PubMed  Google Scholar 

  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):367–373

    Article  PubMed  Google Scholar 

  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):24–29

    PubMed  CAS  Google Scholar 

  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):2236–2239

    Article  PubMed  CAS  Google Scholar 

  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):554–559

    PubMed  Google Scholar 

  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):183–190

    Article  PubMed  CAS  Google Scholar 

  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):148–158

    Article  PubMed  CAS  Google Scholar 

  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):1740–1748

    Article  PubMed  CAS  Google Scholar 

  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):265–273

    Article  PubMed  Google Scholar 

  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):776–779

    Article  PubMed  Google Scholar 

Download references

Funding Sources

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

Author information

Authors and Affiliations

  1. Department of Pediatrics, Children’s Hospital of Philadelphia, 3535 Market Street, Room 1564, Philadelphia, PA, 19104, USA

    Lindsay M. Griffin, Babette S. Zemel, Rachel J. Wetzsteon & Mary B. Leonard

  2. Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Heidi J. Kalkwarf & C. Frederic Strife

  3. Department of Biostatistics and Epidemiology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA

    Justine Shults & Mary B. Leonard

Authors
  1. Lindsay M. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heidi J. Kalkwarf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Babette S. Zemel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Justine Shults
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rachel J. Wetzsteon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Frederic Strife
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mary B. Leonard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mary B. Leonard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Griffin, L.M., Kalkwarf, H.J., Zemel, B.S. et al. Assessment of dual-energy x-ray absorptiometry measures of bone health in pediatric chronic kidney disease. Pediatr Nephrol 27, 1139–1148 (2012). https://doi.org/10.1007/s00467-012-2116-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00467-012-2116-x

Keywords

Search

Navigation