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Bone micro-architecture of elite alpine skiers is not reflected by bone mineral density

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Abstract

Summary

Bone quality is affected by muscle forces and external forces. We investigated how micro-architecture is influenced in elite alpine skiers who have received high loading levels throughout their adolescent bone development. Bone strength was higher in skiers, likely due to external forces, but muscle forces may also be a significant contributor.

Introduction

Impact loading and muscle forces affect bone quality, but little is known about how they influence 3 dimensional aspects of bone structure. This study investigated bone quality in female and male elite alpine skiers using high-resolution peripheral quantitative computed tomography (HR-pQCT).

Methods

HR-pQCT at the distal radius and tibia, whole-body lean mass, and muscle strength were assessed in 10 female (22.7 ± 3.9 years) and 12 male (25.5 ± 3.3 years) Canadian national alpine team athletes and compared to recreationally active female (N = 10, 23.8 ± 3.2 years) and male (N = 12; 23.7 ± 3.6 years) control subjects. HR-pQCT standard parameters and customized cortical and finite element (FE) analyses were performed and analyzed using one-way ANOVA and Pearson’s correlation.

Results

Male and female skiers had stronger bones than controls at radius (38–49 %, p < 0.001) and tibia (24–28 %, p < 0.001). This result was not consistently reflected by total bone mineral density (BMD) because higher trabecular BMD occurred in parallel with lower cortical BMD, which was due to a redistribution of mineral leading to a shift of the endocortical margin toward a thicker cortex. The endocortical regional adaptation was likely responsible for the greater strength of the athletes’ bones. Lean mass and muscle strength was 29 to 90 % greater (p < 0.001) in athletes compared to controls. Good associations between muscle strength and FE-estimated bone strength were found (r = 0.63 to 0.80; p < 0.001), although micro-architecture was more strongly associated with muscle outcomes in females than males.

Conclusions

Higher bone strength in elite alpine skiers is achieved through micro-architectural adaptation that is not apparent by BMD measurements alone. The improved micro-architecture at radius and tibia suggests that muscle forces may play an important role in bone adaptation.

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References

  1. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001). Osteoporosis prevention, diagnosis, and therapy. JAMA 14;285(6):785–795

  2. Ruff C, Holt B, Trinkaus E (2006) Who’s afraid of the big bad Wolff?: "Wolff’s law" and bone functional adaptation. Am J Phys Anthropol 129:484–498

    Article  PubMed  Google Scholar 

  3. Nikander R, Sievanen H, Heinonen A, Karstila T, Kannus P (2008) Load-specific differences in the structure of femoral neck and tibia between world-class moguls skiers and slalom skiers. Scand J Med Sci Sports 18:145–153

    Article  CAS  PubMed  Google Scholar 

  4. Lanyon LE, Hampson WG, Goodship AE, Shah JS (1975) Bone deformation recorded in vivo from strain gauges attached to the human tibial shaft. Acta Orthop Scand 46:256–268

    Article  CAS  PubMed  Google Scholar 

  5. Judex S, Carlson KJ (2009) Is bone’s response to mechanical signals dominated by gravitational loading? Med Sci Sports Exerc 41:2037–2043

    Article  PubMed  Google Scholar 

  6. Kohrt WM, Barry DW, Schwartz RS (2009) Muscle forces or gravity: what predominates mechanical loading on bone? Med Sci Sports Exerc 41:2050–2055

    Article  PubMed Central  PubMed  Google Scholar 

  7. Lang TF (2011) The bone-muscle relationship in men and women. J Osteoporos 2011:702735

    PubMed Central  PubMed  Google Scholar 

  8. Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK (2011) Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-based HR-pQCT study. J Bone Miner Res 26:50–62

    Article  PubMed  Google Scholar 

  9. Kirmani S, Christen D, van Lenthe GH et al (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24:1033–1042

    Article  PubMed Central  PubMed  Google Scholar 

  10. Aaron JE, Makins NB, Sagreiya K (1987) The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop Relat Res 215:260–271

    PubMed  Google Scholar 

  11. Dalzell N, Kaptoge S, Morris N, Berthier A, Koller B, Braak L, van Rietbergen B, Reeve J (2009) Bone micro-architecture and determinants of strength in the radius and tibia: age-related changes in a population-based study of normal adults measured with high-resolution pQCT. Osteoporos Int

  12. Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, Peterson JM, Melton LJ 3rd (2006) Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res 21:124–131

    Article  PubMed Central  PubMed  Google Scholar 

  13. Yee AG, Mote CD (1997) Forces and moments at the knee and boot top: models for an Alpine skiing population. J Appl Biomech 13:373–384

    Google Scholar 

  14. Supej M, Kipp R, Holmberg HC (2011) Mechanical parameters as predictors of performance in alpine World Cup slalom racing. Scand J Med Sci Sports 21:e72–e81

    Article  CAS  PubMed  Google Scholar 

  15. Klous M, Muller E, Schwameder H (2012) Three-dimensional knee joint loading in alpine skiing: a comparison between a carved and a skidded turn. J Appl Biomech 28:655–664

    PubMed  Google Scholar 

  16. MacNeil JA, Boyd SK (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213

    Article  PubMed  Google Scholar 

  17. Hagstromer M, Oja P, Sjostrom M (2006) The International Physical Activity Questionnaire (IPAQ): a study of concurrent and construct validity. Public Health Nutr 9:755–762

    Article  PubMed  Google Scholar 

  18. Barr SI (1994) Associations of social and demographic variables with calcium intakes of high school students. J Am Diet Assoc 94(260–266):269, quiz 267–268

    Google Scholar 

  19. Montomoli M, Gonnelli S, Giacchi M, Mattei R, Cuda C, Rossi S, Gennari C (2002) Validation of a food frequency questionnaire for nutritional calcium intake assessment in Italian women. Eur J Clin Nutr 56:21–30

    Article  CAS  PubMed  Google Scholar 

  20. MacNeil JA, Boyd SK (2007) Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 29:1096–1105

    Article  PubMed  Google Scholar 

  21. Burrows M, Liu D, Perdios A, Moore S, Mulpuri K, McKay H (2010) Assessing bone microstructure at the distal radius in children and adolescents using HR-pQCT: a methodological pilot study. J Clin Densitometry : Off J Int Soc Clin Densitom 13:451–455

    Article  Google Scholar 

  22. Pauchard Y, Liphardt AM, Macdonald HM, Hanley DA, Boyd SK (2012) Quality control for bone quality parameters affected by subject motion in high-resolution peripheral quantitative computed tomography. Bone 50:1304–1310

    Article  PubMed  Google Scholar 

  23. Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S (2012) Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone 50:111–118

    Article  CAS  PubMed  Google Scholar 

  24. Laib A, Hauselmann HJ, Rüegsegger P (1998) In vivo high resolution 3D-QCT of the human forearm. Technol Health Care 6:329–337

    CAS  PubMed  Google Scholar 

  25. Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515

    Article  CAS  PubMed  Google Scholar 

  26. MacNeil JA, Boyd SK (2008) Improved reproducibility of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 30:792–799

    Article  PubMed  Google Scholar 

  27. Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK (2007) Automatic segmentation based on a dual threshold technique for in vivo micro-CT bone analysis. Bone 41:505–515

    Article  PubMed  Google Scholar 

  28. Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK (2010) Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone 47:519–528

    Article  PubMed Central  PubMed  Google Scholar 

  29. Hildebrand T, Ruegsegger P (1997) Quantification of bone microarchitecture with the structure model index. Comp Methods Biomech Biomed Eng 1:15–23

    Article  Google Scholar 

  30. Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P (2002) Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone 30:842–848

    Article  CAS  PubMed  Google Scholar 

  31. Ribom E, Ljunggren O, Piehl-Aulin K, Ljunghall S, Bratteby LE, Samuelson G, Mallmin H (2004) Muscle strength correlates with total body bone mineral density in young women but not in men. Scand J Med Sci Sports 14:24–29

    Article  CAS  PubMed  Google Scholar 

  32. Nordstrom P, Lorentzon R (1996) Site-specific bone mass differences of the lower extremities in 17-year-old ice hockey players. Calcif Tissue Int 59:443–448

    Article  CAS  PubMed  Google Scholar 

  33. Alfredson H, Nordstrom P, Lorentzon R (1996) Total and regional bone mass in female soccer players. Calcif Tissue Int 59:438–442

    Article  CAS  PubMed  Google Scholar 

  34. Berg HE, Eiken O (1999) Muscle control in elite alpine skiing. Med Sci Sports Exerc 31:1065–1067

    Article  CAS  PubMed  Google Scholar 

  35. Liu PY, Ilich JZ, Brummel-Smith K, Ghosh S (2014) New insight into fat, muscle and bone relationship in women: determining the threshold at which body fat assumes negative relationship with bone mineral density. Int J Prev Med 5:1452–1463

    PubMed Central  PubMed  Google Scholar 

  36. Pettersson U, Nordstrom P, Lorentzon R (1999) A comparison of bone mineral density and muscle strength in young male adults with different exercise level. Calcif Tissue Int 64:490–498

    Article  CAS  PubMed  Google Scholar 

  37. Rantalainen T, Nikander R, Daly RM, Heinonen A, Sievanen H (2011) Exercise loading and cortical bone distribution at the tibial shaft. Bone 48:786–791

    Article  CAS  PubMed  Google Scholar 

  38. Schnackenburg KE, Macdonald HM, Ferber R, Wiley JP, Boyd SK (2011) Bone quality and muscle strength in female athletes with lower limb stress fractures. Med Sci Sports Exerc 43:2110–2119

    Article  PubMed  Google Scholar 

  39. Kazakia GJ, Nirody JA, Bernstein G, Sode M, Burghardt AJ, Majumdar S (2013) Age- and gender-related differences in cortical geometry and microstructure: improved sensitivity by regional analysis. Bone 52:623–631

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) and the Canadian Institutes of Health Research (CIHR). We are thankful for all participating athletes from Alpine Canada as well as the support from their coaches and the Exercise Physiology group at the Roger Jackson Center for Health and Wellness Research, University of Calgary. Thank you to our control subjects for participating in the study.

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Correspondence to S. K. Boyd.

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Liphardt, AM., Schipilow, J.D., Macdonald, H.M. et al. Bone micro-architecture of elite alpine skiers is not reflected by bone mineral density. Osteoporos Int 26, 2309–2317 (2015). https://doi.org/10.1007/s00198-015-3133-y

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