Skip to main content
Erschienen in: Osteoporosis International 2/2017

12.10.2016 | Original Article

Meagre effects of disuse on the human fibula are not explained by bone size or geometry

verfasst von: A. Ireland, R. F. Capozza, G. R. Cointry, L. Nocciolino, J. L. Ferretti, J. Rittweger

Erschienen in: Osteoporosis International | Ausgabe 2/2017

Einloggen, um Zugang zu erhalten

Abstract

Summary

Fibula response to disuse is unknown; we assessed fibula bone in spinal cord injury (SCI) patients and able-bodied counterparts. Group differences were smaller than in the neighbouring tibia which could not be explained by bone geometry. Differential adaptation of the shank bones may indicate previously unknown mechanoadaptive behaviours of bone.

Introduction

The fibula supports only a small and highly variable proportion of shank compressive load (−8 to +19 %), and little is known about other kinds of stresses. Hence, whilst effects of habitual loading on tibia are well-known, fibula response to disuse is difficult to predict.

Methods

Therefore, we assessed fibular bone strength using peripheral quantitative computed tomography (pQCT) at 5 % increments from 5 to 90 % distal-proximal tibia length in nine participants with long-term spinal cord injury (SCI; age 39.2 ± 6.2 years, time since injury 17.8 ± 7.4 years), representing a cross-sectional model of long-term disuse and in nine able-bodied counterparts of similar age (39.6 ± 7.8 years), height and mass.

Results

There was no group difference in diaphyseal fibula total bone mineral content (BMC) (P = 0.22, 95 % CIs -7.4 % to -13.4 % and +10.9 % to +19.2 %). Site by group interactions (P < 0.001) revealed 27 and 22 % lower BMC in SCI at 5 and 90 % (epiphyseal) sites only. Cortical bone geometry differed at mid and distal diaphysis, with lower endocortical circumference and greater cortical thickness in SCI than able-bodied participants in this region only (interactions both P < 0.01). Tibia bone strength was also assessed; bone by group interactions showed smaller group differences in fibula than tibia for all bone parameters, with opposing effects on distal diaphysis geometry in the two bones (all Ps < 0.001).

Conclusions

These results suggest that the structure of the fibula diaphysis is not heavily influenced by compressive loading, and only mid and distal diaphysis are influenced by bending and/or torsional loads. The fibula is less influenced by disuse than the tibia, which cannot satisfactorily be explained by differences in bone geometry or relative changes in habitual loading in disuse. Biomechanical study of the shank loading environment may give new information pertaining to factors influencing bone mechanoadaptation.
Literatur
1.
Zurück zum Zitat Funk JR, Rudd RW, Kerrigan JR, Crandall JR (2007) The line of action in the tibia during axial compression of the leg. J Biomech 40:2277–2282CrossRefPubMed Funk JR, Rudd RW, Kerrigan JR, Crandall JR (2007) The line of action in the tibia during axial compression of the leg. J Biomech 40:2277–2282CrossRefPubMed
2.
Zurück zum Zitat Wang Q, Whittle M, Cunningham J, Kenwright J (1996) Fibula and its ligaments in load transmission and ankle joint stability. Clin Orthop Relat Res:261–270 Wang Q, Whittle M, Cunningham J, Kenwright J (1996) Fibula and its ligaments in load transmission and ankle joint stability. Clin Orthop Relat Res:261–270
3.
Zurück zum Zitat Thambyah A, Pereira BP (2006) Mechanical contribution of the fibula to torsion stiffness in the lower extremity. Clin Anat 19:615–620CrossRefPubMed Thambyah A, Pereira BP (2006) Mechanical contribution of the fibula to torsion stiffness in the lower extremity. Clin Anat 19:615–620CrossRefPubMed
4.
Zurück zum Zitat Cointry GR, Nocciolino L, Ireland A, Hall NM, Kriechbaumer A, Ferretti JL, Rittweger J, Capozza RF (2015) Structural differences in cortical shell properties between upper and lower human fibula as described by pQCT serial scans. A biomechanical interpretation. Bone 90:185–194 Cointry GR, Nocciolino L, Ireland A, Hall NM, Kriechbaumer A, Ferretti JL, Rittweger J, Capozza RF (2015) Structural differences in cortical shell properties between upper and lower human fibula as described by pQCT serial scans. A biomechanical interpretation. Bone 90:185–194
5.
Zurück zum Zitat Alho A, Høiseth A (1991) Bone mass distribution in the lower leg. A quantitative computed tomographic study of 36 individuals. Acta Orthop Scand 62:468–470CrossRefPubMed Alho A, Høiseth A (1991) Bone mass distribution in the lower leg. A quantitative computed tomographic study of 36 individuals. Acta Orthop Scand 62:468–470CrossRefPubMed
6.
Zurück zum Zitat Taddei F, Balestri M, Rimondi E, Viceconti M, Manfrini M (2009) Tibia adaptation after fibula harvesting: an in vivo quantitative study. Clin Orthop Relat Res 467:2149–2158CrossRefPubMedPubMedCentral Taddei F, Balestri M, Rimondi E, Viceconti M, Manfrini M (2009) Tibia adaptation after fibula harvesting: an in vivo quantitative study. Clin Orthop Relat Res 467:2149–2158CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Marchi D, Shaw CN (2011) Variation in fibular robusticity reflects variation in mobility patterns. J Hum Evol 61:609–616CrossRefPubMed Marchi D, Shaw CN (2011) Variation in fibular robusticity reflects variation in mobility patterns. J Hum Evol 61:609–616CrossRefPubMed
8.
Zurück zum Zitat Pećina M, Ruszkowsky I, Muftić O, Antičević D (1982) The fibula in clinical and experimental evaluation of the theory on functional adaptation of bone. Collegium Antropologicum 6:197–206 Pećina M, Ruszkowsky I, Muftić O, Antičević D (1982) The fibula in clinical and experimental evaluation of the theory on functional adaptation of bone. Collegium Antropologicum 6:197–206
9.
Zurück zum Zitat Coupaud S, McLean AN, Purcell M, Fraser MH, Allan DB (2015) Decreases in bone mineral density at cortical and trabecular sites in the tibia and femur during the first year of spinal cord injury. Bone 74:69–75CrossRefPubMed Coupaud S, McLean AN, Purcell M, Fraser MH, Allan DB (2015) Decreases in bone mineral density at cortical and trabecular sites in the tibia and femur during the first year of spinal cord injury. Bone 74:69–75CrossRefPubMed
10.
Zurück zum Zitat Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H (2004) Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 34:869–880CrossRefPubMed Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H (2004) Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 34:869–880CrossRefPubMed
11.
Zurück zum Zitat Rittweger J, Goosey-Tolfrey VL, Cointry G, Ferretti JL (2010) Structural analysis of the human tibia in men with spinal cord injury by tomographic (pQCT) serial scans. Bone 47:511–518CrossRefPubMed Rittweger J, Goosey-Tolfrey VL, Cointry G, Ferretti JL (2010) Structural analysis of the human tibia in men with spinal cord injury by tomographic (pQCT) serial scans. Bone 47:511–518CrossRefPubMed
12.
13.
Zurück zum Zitat Rittweger J, Frost HM, Schiessl H, Ohshima H, Alkner B, Tesch P, Felsenberg D (2005) Muscle atrophy and bone loss after 90 days’ bed rest and the effects of flywheel resistive exercise and pamidronate: results from the LTBR study. Bone 36:1019–1029CrossRefPubMed Rittweger J, Frost HM, Schiessl H, Ohshima H, Alkner B, Tesch P, Felsenberg D (2005) Muscle atrophy and bone loss after 90 days’ bed rest and the effects of flywheel resistive exercise and pamidronate: results from the LTBR study. Bone 36:1019–1029CrossRefPubMed
14.
Zurück zum Zitat Kern DS, Semmler JG, Enoka RM (2001) Long-term activity in upper- and lower-limb muscles of humans. J Appl Physiol 91:2224–2232PubMed Kern DS, Semmler JG, Enoka RM (2001) Long-term activity in upper- and lower-limb muscles of humans. J Appl Physiol 91:2224–2232PubMed
15.
Zurück zum Zitat Rittweger J, Michaelis I, Giehl M, Wüsecke P, Felsenberg D (2004) Adjusting for the partial volume effect in cortical bone analyses of pQCT images. J Musculoskelet Neuronal Interact 4:436–441PubMed Rittweger J, Michaelis I, Giehl M, Wüsecke P, Felsenberg D (2004) Adjusting for the partial volume effect in cortical bone analyses of pQCT images. J Musculoskelet Neuronal Interact 4:436–441PubMed
16.
Zurück zum Zitat Ward KA, Adams JE, Hangartner TN (2005) Recommendations for thresholds for cortical bone geometry and density measurement by peripheral quantitative computed tomography. Calcif Tissue Int 77:275–280CrossRefPubMed Ward KA, Adams JE, Hangartner TN (2005) Recommendations for thresholds for cortical bone geometry and density measurement by peripheral quantitative computed tomography. Calcif Tissue Int 77:275–280CrossRefPubMed
17.
Zurück zum Zitat Hangartner TN, Gilsanz V (1996) Evaluation of cortical bone by computed tomography. J Bone Miner Res 11:1518–1525CrossRefPubMed Hangartner TN, Gilsanz V (1996) Evaluation of cortical bone by computed tomography. J Bone Miner Res 11:1518–1525CrossRefPubMed
18.
Zurück zum Zitat Rittweger J, Beller G, Ehrig J et al (2000) Bone-muscle strength indices for the human lower leg. Bone 27:319–326CrossRefPubMed Rittweger J, Beller G, Ehrig J et al (2000) Bone-muscle strength indices for the human lower leg. Bone 27:319–326CrossRefPubMed
19.
Zurück zum Zitat Rittweger J, Simunic B, Bilancio G, De Santo NG, Cirillo M, Biolo G, Pisot R, Eiken O, Mekjavic IB, Narici M (2009) Bone loss in the lower leg during 35 days of bed rest is predominantly from the cortical compartment. Bone 44:612–618CrossRefPubMed Rittweger J, Simunic B, Bilancio G, De Santo NG, Cirillo M, Biolo G, Pisot R, Eiken O, Mekjavic IB, Narici M (2009) Bone loss in the lower leg during 35 days of bed rest is predominantly from the cortical compartment. Bone 44:612–618CrossRefPubMed
20.
Zurück zum Zitat Rantalainen T, Duckham RL, Suominen H, Heinonen A, Alén M, Korhonen MT (2014) Tibial and fibular mid-shaft bone traits in young and older sprinters and non-athletic men. Calcif Tissue Int 95:132–140CrossRefPubMed Rantalainen T, Duckham RL, Suominen H, Heinonen A, Alén M, Korhonen MT (2014) Tibial and fibular mid-shaft bone traits in young and older sprinters and non-athletic men. Calcif Tissue Int 95:132–140CrossRefPubMed
21.
Zurück zum Zitat Rantalainen T, Nikander R, Heinonen A, Suominen H, Sievänen H (2010) Direction-specific diaphyseal geometry and mineral mass distribution of tibia and fibula: a pQCT study of female athletes representing different exercise loading types. Calcif Tissue Int 86:447–454CrossRefPubMed Rantalainen T, Nikander R, Heinonen A, Suominen H, Sievänen H (2010) Direction-specific diaphyseal geometry and mineral mass distribution of tibia and fibula: a pQCT study of female athletes representing different exercise loading types. Calcif Tissue Int 86:447–454CrossRefPubMed
22.
Zurück zum Zitat Parfitt AM (2002) Misconceptions (2): turnover is always higher in cancellous than in cortical bone. Bone 30:807–809CrossRefPubMed Parfitt AM (2002) Misconceptions (2): turnover is always higher in cancellous than in cortical bone. Bone 30:807–809CrossRefPubMed
23.
24.
Zurück zum Zitat Noble BS, Peet N, Stevens HY, Brabbs A, Mosley JR, Reilly GC, Reeve J, Skerry TM, Lanyon LE (2003) Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol 284:C934–C943CrossRefPubMed Noble BS, Peet N, Stevens HY, Brabbs A, Mosley JR, Reilly GC, Reeve J, Skerry TM, Lanyon LE (2003) Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol 284:C934–C943CrossRefPubMed
25.
Zurück zum Zitat Rodríguez JI, Palacios J, García-Alix A, Pastor I, Paniagua R (1988) Effects of immobilization on fetal bone development. A morphometric study in newborns with congenital neuromuscular diseases with intrauterine onset. Calcif Tissue Int 43:335–339CrossRefPubMed Rodríguez JI, Palacios J, García-Alix A, Pastor I, Paniagua R (1988) Effects of immobilization on fetal bone development. A morphometric study in newborns with congenital neuromuscular diseases with intrauterine onset. Calcif Tissue Int 43:335–339CrossRefPubMed
26.
Zurück zum Zitat Biggin A, Briody JN, Ramjan KA, Middleton A, Waugh MC, Munns CF (2013) Evaluation of bone mineral density and morphology using pQCT in children after spinal cord injury. Dev Neurorehabil 16:391–397CrossRefPubMed Biggin A, Briody JN, Ramjan KA, Middleton A, Waugh MC, Munns CF (2013) Evaluation of bone mineral density and morphology using pQCT in children after spinal cord injury. Dev Neurorehabil 16:391–397CrossRefPubMed
27.
Zurück zum Zitat Cullen DM, Smith RT, Akhter MP (2001) Bone-loading response varies with strain magnitude and cycle number. J Appl Physiol 91:1971–1976PubMed Cullen DM, Smith RT, Akhter MP (2001) Bone-loading response varies with strain magnitude and cycle number. J Appl Physiol 91:1971–1976PubMed
28.
Zurück zum Zitat Turner CH, Owan I, Takano Y (1995) Mechanotransduction in bone: role of strain rate. Am J Phys 269:E438–E442 Turner CH, Owan I, Takano Y (1995) Mechanotransduction in bone: role of strain rate. Am J Phys 269:E438–E442
29.
Zurück zum Zitat Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, Fuchs RK (2014) Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci U S A 111(14):5337–5342 Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, Fuchs RK (2014) Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci U S A 111(14):5337–5342
30.
Zurück zum Zitat Ireland A, Maden-Wilkinson T, Ganse B, Degens H, Rittweger J (2014) Effects of age and starting age upon side asymmetry in the arms of veteran tennis players: a cross-sectional study. Osteoporos Int 25:1389–1400CrossRefPubMed Ireland A, Maden-Wilkinson T, Ganse B, Degens H, Rittweger J (2014) Effects of age and starting age upon side asymmetry in the arms of veteran tennis players: a cross-sectional study. Osteoporos Int 25:1389–1400CrossRefPubMed
31.
Zurück zum Zitat Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2008) Osteocyte morphology in fibula and calvaria—is there a role for mechanosensing? Bone 43:452–458CrossRefPubMed Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2008) Osteocyte morphology in fibula and calvaria—is there a role for mechanosensing? Bone 43:452–458CrossRefPubMed
Metadaten
Titel
Meagre effects of disuse on the human fibula are not explained by bone size or geometry
verfasst von
A. Ireland
R. F. Capozza
G. R. Cointry
L. Nocciolino
J. L. Ferretti
J. Rittweger
Publikationsdatum
12.10.2016
Verlag
Springer London
Erschienen in
Osteoporosis International / Ausgabe 2/2017
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-016-3779-0

Weitere Artikel der Ausgabe 2/2017

Osteoporosis International 2/2017 Zur Ausgabe

Arthropedia

Grundlagenwissen der Arthroskopie und Gelenkchirurgie. Erweitert durch Fallbeispiele, Videos und Abbildungen. 
» Jetzt entdecken

Update Orthopädie und Unfallchirurgie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.