Bone health of children with intestinal failure measured by dual energy X-ray absorptiometry and digital X-ray radiogrammetry

Published:February 21, 2017DOI:


      Background & aims

      Children with intestinal failure (IF) receiving long-term parenteral nutrition (PN) are at risk of developing low bone mineral density (BMD). Next to the dual energy X-ray absorptiometry (DXA) method, digital X-ray radiogrammetry (DXR) using the BoneXpert software has become available to obtain the Bone Health Index (BHI) in hand radiographs. In this study we 1) evaluated the prevalence of low BMD in children with IF using DXA and DXR, 2) compared DXA and DXR results, and 3) aimed to identify factors associated with low BMD.


      A retrospective study was performed including all children with IF between 2000 and 2015 who underwent a DXA measurement and/or a hand radiograph. Z-scores of BMD total body (BMD TB) and lumbar spine (BMD LS), bone mineral apparent density (BMAD) and bone health index (BHI) were collected. A low BMD and low BHI were defined as a Z-score ≤ −2. DXA and DXR results were compared for cases in which a DXA and hand radiograph were performed within a 6 months' interval.


      Forty-six children were included. Overall, 24.3% of the children had a low BMD at the first DXA at a median age of 6 years; correction for growth failure (n = 6) reduced this to 16.2%. Fifty percent had a low BHI at the first hand radiograph. Median DXA and BHI Z-scores were significantly lower than reference scores. Age, duration of PN and surgical IF were related to lower Z-scores at the first DXA. Paired DXA and DXR results (n = 18) were compared, resulting in a Cohen's kappa of 0.746 (‘substantial’) for BMD TB. Spearman's correlation coefficient for BHI and BMD TB Z-scores was 0.856 (p < 0.001). Hand radiography had a sensitivity of 90% and specificity of 86% (BMD TB).


      Up to 50% of the children had a low BMD. Children with IF have a significantly poorer bone health than the reference population, also after weaning off PN. Bone health assessment by DXA and DXR showed good agreement, especially for Z-scores ≤ −2. DXR assessment using BoneXpert software seems to be feasible for monitoring of bone health in children with IF.



      BHI (bone health index), BMAD (bone mineral apparent density), BMD (bone mineral density), DXA (dual energy X-ray absorptiometry), DXR (digital X-ray radiogrammetry), HFA (height-for-age), IF (intestinal failure), IQR (interquartile range), LS (lumbar spine), PN (parenteral nutrition), SBS (short bowel syndrome), SD (standard deviation), SDS (standard deviation score), TB (total body), TH (target height), WFA (weight-for-age), WFH (weight-for-height)
      To read this article in full you will need to make a payment
      Subscribe to Clinical Nutrition
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Pichler J.
        • Chomtho S.
        • Fewtrell M.
        • Macdonald S.
        • Hill S.M.
        Growth and bone health in pediatric intestinal failure patients receiving long-term parenteral nutrition.
        Am J Clin Nutr. 2013; 97: 1260-1269
        • Diamanti A.
        • Bizzarri C.
        • Basso M.S.
        • Gambarara M.
        • Cappa M.
        • Daniele A.
        • et al.
        How does long-term parenteral nutrition impact the bone mineral status of children with intestinal failure?.
        J Bone Miner Metab. 2010; 28: 351-358
        • Pichler J.
        • Chomtho S.
        • Fewtrell M.
        • Macdonald S.
        • Hill S.
        Body composition in paediatric intestinal failure patients receiving long-term parenteral nutrition.
        Arch Dis Child. 2014; 99: 147-153
        • Mutanen A.
        • Makitie O.
        • Pakarinen M.P.
        Risk of metabolic bone disease is increased both during and after weaning off parenteral nutrition in pediatric intestinal failure.
        Horm Res Paediatr. 2013; 79: 227-235
        • Ubesie A.C.
        • Heubi J.E.
        • Kocoshis S.A.
        • Henderson C.J.
        • Mezoff A.G.
        • Rao M.B.
        • et al.
        Vitamin D deficiency and low bone mineral density in pediatric and young adult intestinal failure.
        J Pediatr Gastroenterol Nutr. 2013; 57: 372-376
        • Bianchi M.L.
        Osteoporosis in children and adolescents.
        Bone. 2007; 41: 486-495
        • Thodberg H.H.
        • van Rijn R.R.
        • Tanaka T.
        • Martin D.D.
        • Kreiborg S.
        A paediatric bone index derived by automated radiogrammetry.
        Osteoporos Int. 2010; 21: 1391-1400
        • Koletzko B.
        • Goulet O.
        • Hunt J.
        • Krohn K.
        • Shamir R.
        • Parenteral Nutrition Guidelines Working G.
        • et al.
        1. Guidelines on paediatric parenteral nutrition of the European Society of Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) and the European Society for Clinical Nutrition and Metabolism (ESPEN), supported by the European Society of paediatric research (ESPR).
        J Pediatr Gastroenterol Nutr. 2005; 41: S1-S87
        • Meijers-Ijselstijn H.
        • Rings E.
        • Tibboel D.
        Het kortedarmsyndroom bij kinderen.
        . 2006; 74: 135-139
        • Talma H.
        • Schönbeck Y.
        • Bakker B.
        • Hirasing R.A.
        • van buuren S.
        Groeidiagrammen 2010. Handleiding bij het meten en wegen van kinderen en het invullen van groeidiagrammen.
        TNO, Leiden2010
        • Schonbeck Y.
        • Talma H.
        • van Dommelen P.
        • Bakker B.
        • Buitendijk S.E.
        • HiraSing R.A.
        • et al.
        The world's tallest nation has stopped growing taller: the height of Dutch children from 1955 to 2009.
        Pediatr Res. 2013; 73: 371-377
        • van der Sluis I.M.
        • de Ridder M.A.
        • Boot A.M.
        • Krenning E.P.
        • de Muinck Keizer-Schrama S.M.
        Reference data for bone density and body composition measured with dual energy x ray absorptiometry in white children and young adults.
        Arch Dis Child. 2002; 87 ([discussion -7]): 341-347
        • Kroger H.
        • Kotaniemi A.
        • Kroger L.
        • Alhava E.
        Development of bone mass and bone density of the spine and femoral neck–a prospective study of 65 children and adolescents.
        Bone Miner. 1993; 23: 171-182
        • Kamphuis M.
        • Obenhuijsen N.H.
        • van Dommelen P.
        • van Buuren S.
        • Verkerk P.H.
        Jeugdgezondheidszorg. [Guideline for preventive child health care: 'Detection and referral criteria in short stature'] Jgz-richtlijn: 'Signalering van en verwijscriteria bij kleine lichaamslengte'.
        Ned Tijdschr Geneeskd. 2010; 154: A2366
        • Gordon C.M.
        • Leonard M.B.
        • Zemel B.S.
        • International Society for Clinical D
        2013 pediatric position development conference: executive summary and reflections.
        J Clin Densitom. 2014; 17: 219-224
        • Blake G.M.
        • Naeem M.
        • Boutros M.
        Comparison of effective dose to children and adults from dual X-ray absorptiometry examinations.
        Bone. 2006; 38: 935-942
        • Huda W.
        • Gkanatsios N.A.
        Radiation dosimetry for extremity radiographs.
        Health Phys. 1998; 75: 492-499
        • Nusman C.M.
        • Anink J.
        • Otten M.H.
        • van Rossum M.A.
        • van Rijn R.R.
        • Maas M.
        • et al.
        Bone health of patients with juvenile idiopathic arthritis: a comparison between dual-energy X-ray absorptiometry and digital X-ray radiogrammetry.
        Eur J Radiol. 2015; 84: 1999-2003
        • Schundeln M.M.
        • Marschke L.
        • Bauer J.J.
        • Hauffa P.K.
        • Schweiger B.
        • Fuhrer-Sakel D.
        • et al.
        A piece of the puzzle: the bone health index of the BoneXpert software reflects cortical bone mineral density in pediatric and adolescent patients.
        PLoS One. 2016; 11: e0151936
        • Thodberg H.H.
        Clinical review: an automated method for determination of bone age.
        J Clin Endocrinol Metab. 2009; 94: 2239-2244
        • Appleman S.S.
        • Kalkwarf H.J.
        • Dwivedi A.
        • Heubi J.E.
        Bone deficits in parenteral nutrition-dependent infants and children with intestinal failure are attenuated when accounting for slower growth.
        J Pediatr Gastroenterol Nutr. 2013; 57: 124-130
        • Fewtrell M.S.
        • Gordon I.
        • Biassoni L.
        • Cole T.J.
        Dual X-ray absorptiometry (DXA) of the lumbar spine in a clinical paediatric setting: does the method of size-adjustment matter?.
        Bone. 2005; 37: 413-419