The aim of this study was to describe longitudinal changes in the fibula bone in response to disuse during the first 12 months of SCI and to compare these changes to those in the tibia. Across epiphyseal and diaphyseal sites, fibular bone loss was less than 50% of that at the corresponding tibia site which supports the results from previous cross-sectional studies [6, 13, 14]. Losses in the tibia and fibula within each participant were not correlated with each other. The loss of BMC that was evident at the fibular shaft (38% and 66%, respectively) contrasts with a previous cross-sectional report that observed no difference in BMC in the fibular shaft in chronic SCI . In both the fibula and tibia, bone losses were more prominent at the distal end compared to the shaft, which supports findings from cross-sectional studies [15, 16].
Previous evidence suggests that: (i) relative changes in fibula loading are greater than those in the tibia, (ii) the fibula supports a substantial portion of shank loading during physical activity and (iii) the fibula is able to change its size and mass dramatically in response to increased loading [2,3,4]. Therefore, it is perhaps surprising that disuse-related bone losses are less than half those in the neighbouring bone. In addition, the lack of correlation reported here between the tibia and fibula suggests further that they are affected by different mechanisms. Evidence for (ii) and (iii) could be considered robust, particularly for (ii) when we consider the occurrence of fibula stress fractures in athletes. However, proposition (i) is based on cadaveric data and, to date, the in vivo loading environment of the fibula is unknown. In addition, previous data describe static loading conditions, and it is well established that the rate of force application is a key determinant of bone mechanoadaptive response. Therefore, assessment of fibula deformation in vivo would improve our understanding of fibula’s mechanoadaptive response.
The mechanisms leading to less pronounced bone loss in the fibula compared to the tibia are not fully understood, but structural differences between the two bones have been considered. The endocortical surface, with its higher rate of bone turnover is larger in the tibia, and previous studies showed that between-site differences in endocortical circumference are strongly correlated with site-specific loss in the tibia [15, 8]. However, when normalised to bone size the surface:area ratio is greater in the fibula than in the equivalent sites in the tibia suggesting that this does not contribute to observed inter-bone differences. For the two diaphyseal sites, the percentage loss was identical. However, it was statistically evident at the 66% and not at the 38% due to the greater dispersion in BMC changes at 38% which appeared to be related to one outlier.
Divergent responses of the distal tibia and fibula to disuse could alternatively be explained in part by the greater trabecular component in the distal tibia, that is known to show a more rapid response to disuse (in absolute terms) compared to the cortical component [7, 16]. In secondary analyses, we considered the relative proportions of trabecular and cortical bone in addition to relative losses in the two bone regions. At the distal tibia, 31% of bone mass was trabecular whereas the proportion was negligible in the fibula. However, percentage bone loss was higher in the distal tibia cortical component than in the distal fibula, and these losses were also more than twice as large as those observed in the cortical component of the distal fibula. When considering that at both tibia and fibula shaft sites the bone was almost entirely cortical, it seems clear that the relative proportions of trabecular and cortical bone cannot explain the differences in bone loss between the tibia and fibula at any site. Whilst caution must be used when assessing cortical bone at the distal tibia using pQCT due to the thin cortical shell and associated partial volume effect, it is reassuring that our findings of similar loss in cortical and trabecular components is similar to a previous report using high-resolution pQCT .
That modest fibula response to disuse may explain the low incidence of fibula fractures in patients with SCI, who tend to experience fragility fractures mostly in the distal femur and tibial epiphyses . Moreover, a deeper understanding of the mechanisms that lead to these smaller fibular deficits in disuse could help us develop therapies to mitigate or treat osteoporosis. Understanding these different responses to disuse can also provide more insights into neuro-skeletal interactions that are yet to be fully understood.
To the best of our knowledge, this study is the first to explore the fibula’s response to disuse following SCI longitudinally. Within-individual comparisons enabled a characterisation of disuse-related loss in the fibula which has not been possible in previous cross-sectional studies. However, the absence of an uninjured control group in this longitudinal study, prevented a direct comparison to determine whether the bone losses observed in the fibula differed from typical age-related changes. Whilst tibial changes are clearly far greater than those observed in controls , no comparable data exists for the fibula. In the only longitudinal study of the fibula bone in older adult athletes (in whom disuse does not contribute), the fibula changes in the shaft are not entirely dissimilar . Therefore, further controlled studies or alternative disuse models should be examined.