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Outcome of muscle and bone development in congenital heart disease

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Abstract

Muscles and bones of patients with congenital heart disease (CHD) are subject to various potentially deleterious influences during growth. The aim of the present study was to analyse the outcome of bone and muscle parameters in adolescents and young adults with a spectrum of CHD. Bone and muscle parameters of the forearm were examined at two standard sites, 4% and 65%, in 29 adolescents and young adults with CHD, aged 14–24 years, by quantitative computed tomography. For the entire study population, bone and muscle parameters did not deviate significantly from the reference values except for age- and gender-corrected body height (ASDS-height: −0.6±1.2, p=0.01). Both age- and gender- and height- and gender-corrected (HSDS) abnormal bone mass (BMC) was found at the distal radius in patients with Fontan repair (ASDS-BMC4%:−1.5±0.9, p=0.008; HSDS-BMC4%:−1.2±1.0, p=0.05) and in those in NYHA class III (ASDS-BMC4%:−1.3±0.4, p=0.001; HSDS-BMC4%:−1.4±0.5, p=0.004). There was minimal overlap between Fontan patients (n=6) and NYHA class III (5 Fontan patients were in NYHA class I or II). In conclusion, most patients with CHD show a normal muscle and bone development in proportion to their reduced body height. Further follow-up is required to determine whether patients in a worse clinical status (NYHA III) and those with single ventricle physiology are at increased risk of osteoporosis and fractures.

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Abbreviations

ASDS:

Age and sex-specific standard deviation score

BMC4%:

Bone mass at the 4%-measuring point

BMC65%/MA:

Ratio of bone mass at the 65%-measuring point and muscle cross-sectional area

BMDtrab4%:

Trabecular volumetric bone mineral density at the 4%-measuring point

CAHD:

Complex acyanotic heart disease

CCHD:

Complex cyanotic heart disease with no surgery or only palliation

CCHDrs:

Complex cyanotic heart disease anatomically or functionally corrected

CHD:

Congenital heart disease

DXA:

Dual energy x-ray absorptiometry

HSDS:

Body height and sex-specific standard deviation score

ID:

Isolated defects

MA:

Muscle cross-sectional area

pQCT:

Peripheral quantitative computed tomography

SSI65%:

Bone strength strain index at the 65%-measuring point

tcSO2:

Transcutaneous oxygen saturation

References

  1. Arnett TR, Gibbons DC, Utting JC, Orriss IR, Hoebertz A, Rosendaal M, Meghji S (2003) Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol 196:2–8

    Article  PubMed  CAS  Google Scholar 

  2. World Health Organization (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: report of a WHO study group (1994). WHO Technical Report Series 843

  3. Bailey DA, Wedge JH, McCulloch RG, Martin AD, Bernhardson SC (1989) Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am 71:1225–1231

    PubMed  CAS  Google Scholar 

  4. Boot AM, de Ridder MA, Pols HA, Krenning EP, de Muinck Keizer-Schrama SM (1997) Bone mineral density in children and adolescents: relation to puberty, calcium intake and physical activity. J Endocrinol Metab 82:57–62

    Article  CAS  Google Scholar 

  5. Caulfield LE, Himes JH, Rivera JA (1995) Nutritional supplementation during early childhood and bone mineralization during adolescence. J Nutr 125:1104–1110

    Google Scholar 

  6. Christ E, Linka A, Junga G, Odermatt M, Steinert H, Kiowski W, Schmid C (1996) Bone density and laboratory parameters of bone metabolism in patients with terminal heart disease. Schweiz Med Wochenschr 126(37):1553–1559

    PubMed  CAS  Google Scholar 

  7. Consensus Development Conference (1991) Diagnosis, prophylaxis and treatment of osteoporosis. Am J Med 90:170–210

    Google Scholar 

  8. Fricke O, Weidler J, Tutlewski B, Schoenau E (2005) Mechanography-a new device for the assessment of muscle function in pediatrics. Pediatr Res (in press)

  9. Frost HM, Ferretti JL, Jee WS (1998) Perspectives: some roles of mechanical usage, muscle strength and the mechanostat in skeletal physiology, disease and research. Calcif Tissue Int 62:1–7

    Article  PubMed  CAS  Google Scholar 

  10. Frost HM, Schoenau E (2000) The “Muscle-Bone Unit” in children and adolescents: a 2000 overview. J Ped Endocrin 13:571–590

    CAS  Google Scholar 

  11. Garcia Delgado I, Gil-Fraguas L, Robles E, Martinez G, Hawkins F (2000) Clinical factors associated with bone mass loss previous cardiac transplantation. Med Clin (Barc) 114:761–764

    CAS  Google Scholar 

  12. Hansen MA, Overgaard K, Riis B, Christiansen C (1991) Role of peak bone mass and bone loss in postmenopausal osteoporosis:12 year study. BMJ 3030:961–964

    Google Scholar 

  13. Kerpel-Fronius E, Kiss S, Kardos G (1977) Somatomedin and growth hormone in children with retarded growth and atrophy due to congenital heart disease or malabsorption. Monatsschr Kinderheilkd 125:783–786

    PubMed  CAS  Google Scholar 

  14. Kiess W (1993) Störungen des Wachstums. In: Kruse K (ed) Pädiatrische Endokrinologie. Enke Verlag, Stuttgart, pp 188–223

    Google Scholar 

  15. Lee AH, Mull RL, Keenan GF, Callegari PE, Dalinka MK, Eisen HJ, Mancini DM, Di Sesa VJ, Attie MF (1994) Osteoporosis and bone morbidity in cardiac transplant recipients. Am J Med 96:35–41

    Article  PubMed  CAS  Google Scholar 

  16. Lonzer MD, Imrie R, Rogers D, Worley D, Licata A, Secic M (1996) Effects of heredity, age, weight, puberty, activity and calcium intake on bone mineral density in children. Clin Pediatr 35:185–189

    Article  CAS  Google Scholar 

  17. Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–303

    Article  PubMed  CAS  Google Scholar 

  18. Marshall WA, Tanner JM (1970) Variations in pattern of pubertal changes in boys. Arch Dis Child 45:13–23

    PubMed  CAS  Google Scholar 

  19. Müller-Berghaus J, van Koningsbruggen S, Rietschel E, Mokov E, Michalk D, Schönau E (1997) Bone mineral density, bone strength and muscle strength of cystic fibrosis patients. Exp Clin Endocrinol Diabetes 105(1):103–105

    Google Scholar 

  20. Neu CM, Rauch F, Manz F, Schönau E (2001) Modeling of cross-sectional bone height, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporos Int 12:538–547

    Article  PubMed  CAS  Google Scholar 

  21. Neu CM, Manz F, Rauch F, Merkel A, Schönau E (2001) Bone densities and bone size at the distal radius in healthy children and adolescents: a study using peripheral quantitative computed tomography. Bone 28(2):227–232

    Article  PubMed  CAS  Google Scholar 

  22. Neu CM, Rauch F, Rittweger J, Manz F, Schönau E (2002) Influence of puberty on muscle development at the forearm. AJP Endocrinol Metab 283:103–107

    Google Scholar 

  23. 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 60:837–842

    PubMed  CAS  Google Scholar 

  24. Rauch F, Glorieux FH (2000) Osteoporosis in childhood. In: Henderson JE, Goltzman D (eds) The osteoporosis primer. Cambridge University, Cambridge, pp 221–230

    Google Scholar 

  25. Rauch F, Schoenau E (2001) Changes in bone density during childhood and adolescence: An approach based on bone’s biological organisation. J Bone Miner Res 16:597–604

    Article  PubMed  CAS  Google Scholar 

  26. Rauch F, Neu CM, Manz F, Schönau E (2001) The development of metaphyseal cortex - implications for distal radius fractures during growth. J Bone Min Res 8(16):1547–1555

    Article  Google Scholar 

  27. Rego C, Guerra A, Guardiano M, Esteves P, Pereira J, Aguiar A, Areias JC (2002) Bony density in adolescents after surgical repair of tetralogy of Fallot: a comparative study with healthy adolescents. Cardiol Young 12:531–536

    Article  PubMed  Google Scholar 

  28. Riggs BL, Khosla S, Melton LJ (1999) The assembly of the adult skeleton during growth and maturation: Implications for senile osteoporosis. J Clin Invest 104:671–672

    Article  PubMed  CAS  Google Scholar 

  29. Schiessl H, Ferretti JL, Tysarczyk-Niemeyer G, Willnecker J (1996) Noninvasive bone strength index as analyzed by peripheral quantitative computed tomography (pQCT). In: Schoenau E (ed) Paediatric osteology: new developments in diagnostics and therapy. International congress series 1105. Elsevier Science, Amsterdam, pp 141–146

    Google Scholar 

  30. Schiessl H, Frost HM, Jee WS (1998) Estrogen and bone muscle strength and mass relationships. Bone 22:1–6

    Article  PubMed  CAS  Google Scholar 

  31. Schoenau E, Matkovic V (1997) Paediatric osteology: prevention of osteoporosis – a paediatric task? Elsevier Science, Amsterdam

    Google Scholar 

  32. Schoenau E (1998) The development of the skeletal system in children and the influence of muscular strength. Horm Res 49:27–31

    Article  CAS  Google Scholar 

  33. Schoenau E, Westermann F, Mokow E, Scheidhauer K, Wehrhahn E, Stabrey A, Müller-Berghaus J (1998) The functional muscle-bone-unit in health and disease. In: Schoenau E, Matkovic L (eds) Pediatric osteology: prevention of osteoporosis – a pediatric task? Elsevier Science, Singapore, pp 191–202

    Google Scholar 

  34. Schoenau E (1998) Problems of bone analysis in childhood and adolescence. Pediatr Nephrol 12:420–429

    Article  Google Scholar 

  35. Schoenau E, Neu CM, Mokov E, Manz F (1999) Influence of puberty on the muscle-bone unit in childhood and adolescence. Hormone Res 51(2):66–71

    Google Scholar 

  36. Schoenau E, Neu CM, Mokov E, Wassmer G, Manz F (2000) Influence of puberty on muscle area and cortical bone area of the forearm in boys and girls. J Clin Endocrinol Metab 85:1095–1098

    Article  PubMed  CAS  Google Scholar 

  37. Schoenau E, Neu C, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit. J Bone Miner Res 17:1095–1101

    Article  PubMed  Google Scholar 

  38. Shane E, Mancini D, Aaronson K, Silverberg SJ, Seibel MJ, Addesso V, McMahon DJ (1997) Bone mass, vitamin D deficiency, and hyperparathyroidism in congestive heart failure. Am J Med 103(3):197–207

    Article  PubMed  CAS  Google Scholar 

  39. Slemenda CW, Reister TK, Hui SL, Miller JZ, Chiristian JC (1994) Influences on skeletal mineralization in children and adolescents. Evidence for varying effects of sexual maturation and physical activity. J Pediatr 125:201–207

    Article  PubMed  CAS  Google Scholar 

  40. Tenbrock K, Krupper S, Mokov E, Michalk D, Schönau E, Klein K, Alloli B (2000) Analysis of muscle strength and bone structure in children with renal disease. Pediatr Nephrol 14:669–672

    Article  PubMed  CAS  Google Scholar 

  41. Theintz G, Bucks B, Rizzoli R, Slosman D, Clavien H, Sizonenko PC (1992) Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the level of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 75:1060–1065

    Article  PubMed  CAS  Google Scholar 

  42. Wilhelm G, Felsenberg D, Bogusch B, Willnecker J, Thaten J, Gummert P (1999) Biomechanical examinations for validation of the bone strength strain index SSI, calculated by peripheral quantitative computed tomography. In: Lyritis GP (ed) Musculoskeletal interactions. Basic and clinical aspects. Hylonome Editions, Athen, pp 105–108

    Google Scholar 

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Acknowledgements

We thank the Cologne Fortune Program, Faculty of Medicine, University of Cologne for financial support. The authors are gratefully indebted to Barbara Tutlewski and Angelika Stabrey for their continuing support and help.

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Authors and Affiliations

  1. Department of Pediatric Cardiology, University Hospital of Cologne, Joseph Stelzmann Strasse 9, 50924, Cologne, Germany

    Cordelia Witzel, Narayanswami Sreeram, Sabine Schickendantz & Konrad Brockmeier

  2. Department of Pediatrics, University of Cologne, Cologne, Germany

    Cordelia Witzel & Eckhard Schoenau

  3. Department of Medical Statistics, University of Cologne, Cologne, Germany

    Silke Coburger

Authors
  1. Cordelia Witzel
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  2. Narayanswami Sreeram
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  3. Silke Coburger
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  4. Sabine Schickendantz
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  5. Konrad Brockmeier
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  6. Eckhard Schoenau
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Correspondence to Cordelia Witzel.

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The research reported here has been supported by the Cologne Fortune Programme, Faculty of Medicine, University of Cologne.

None of the authors have any potential, perceived, or real conflicts of interest, especially any financial arrangement, with a company whose product is mentioned in this manuscript.

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Witzel, C., Sreeram, N., Coburger, S. et al. Outcome of muscle and bone development in congenital heart disease. Eur J Pediatr 165, 168–174 (2006). https://doi.org/10.1007/s00431-005-0030-y

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  • DOI: https://doi.org/10.1007/s00431-005-0030-y

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