Bone strength is maintained after 8 months of inactivity in hibernating golden-mantled ground squirrels, Spermophilus lateralis

Abstract

SUMMARYProlonged inactivity leads to disuse atrophy, a loss of muscle and bone mass. Hibernating mammals are inactive for 6-9 months per year but must return to full activity immediately after completing hibernation. This necessity for immediate recovery presents an intriguing conundrum, as many mammals require two to three times the period of inactivity to recover full bone strength. Therefore, if hibernators experience typical levels of bone disuse atrophy during hibernation, there would be inadequate time available to recover during the summer active season. We examined whether there were mechanical consequences as a result of the extended inactivity of hibernation. We dissected femur and tibia bones from squirrels in various stages of the annual hibernation cycle and measured the amount of force required to fracture these bones. Three groups were investigated; summer active animals were captured during the summer and immediately killed, animals in the 1 month detraining group were captured in the summer and killed following a 1-month period of restricted mobility, hibernating animals were killed after 8 months of inactivity. A three-point bend test was employed to measure the force required to break the bones. Apparent flexural strength and apparent flexural modulus (material stiffness) were calculated for femurs. There were no differences between groups for femur fracture force, tibia fracture force, or femur flexural strength. Femur flexural modulus was significantly less for the 1 month detraining group than for the hibernation and summer active groups. Thus, hibernators seem resistant to the deleterious effects of prolonged inactivity during the winter. However, they may be susceptible to immobilization-induced bone loss during the summer.

Thirteen-lined ground squirrels (Ictidomys tridecemlineatus) show microstructural bone loss during hibernation but preserve bone macrostructural geometry and strength

“…We saw no evidence of macrostructural cortical bone loss in hibernating ground squirrels, since cortical bone geometrical properties and whole bone mechanical properties were comparable between hibernating and active squirrels (Table1). These results, which are in agreement with a recent finding on the preservation of bone strength in hibernating golden-mantled squirrels (Utz et al, 2009), suggest that 13-lined ground squirrels have adapted to prevent disuse-induced macrostructural cortical bone loss, and that hibernation does not lead to an increased risk of bone fracture upon remobilization. It is, however, unclear whether all hibernating animals experience similar skeletal responses to disuse.…”

“…Ultimate load, ultimate stress and stiffness of the femurs were not affected by hibernation, suggesting that overall, cortical bone seems to be resistant to disuseinduced bone loss in 13-lined ground squirrels, as was recently demonstrated in golden-mantled ground squirrels (Utz et al, 2009). Therefore, small hibernators, including ground squirrels, may be useful models for investigating biological mechanisms of cortical bone preservation during disuse.…”

“…decreased bone mineral content and decreased cortical bone thickness) during cold stress and hibernation (Bruce and Wiebers, 1970;Haller and Zimny, 1977;Steinberg et al, 1981;Kwiecinski et al, 1987). However, a recent study on golden-mantled ground squirrels showed cortical bone strength was not affected by hibernation (Utz et al, 2009). Quantitative studies of bone geometry, microstructure and mineralization are needed to address these differing reports and to better understand the effects of physical inactivity on skeletal integrity in small mammalian hibernators.…”

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

“…Interestingly, summer (i.e. awake) squirrels that experienced restricted mobility exhibited reduced flexural modulus (stiffness) of the femur when compared with active summer squirrels (Utz et al, 2009). …”

“…Early studies suggested that small hibernating mammals such as bats, ground squirrels and hamsters might experience bone loss during hibernation (Kayser and Frank, 1963;Mayer and Bernick, 1959;Whalen et al, 1972). However, more recent data from hibernating S. lateralis squirrels indicate that bone strength and stiffness are unaffected by winter inactivity (Utz et al, 2009). Interestingly, summer (i.e.…”