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

Abstract

SUMMARYLack of activity causes bone loss In most animals. Hibernating bears have physiological processes to prevent cortical and trabecular bone loss associated with reduced physical activity, but different mechanisms of torpor among hibernating species may lead to differences in skeletal responses to hibernation. There are conflicting reports regarding whether small mammals experience bone loss during hibernation. To investigate this phenomenon, we measured cortical and trabecular bone properties in physically active and hibernating juvenile and adult 13-lined ground squirrels (Ictidomys tridecemlineatus, previous genus name Spermophilus). Cortical bone geometry, strength and mineral content were similar in hibernating compared with active squirrels, suggesting that hibernation did not cause macrostructural cortical bone loss. Osteocyte lacunar size increased (linear regression, P0.001) over the course of hibernation in juvenile squirrels, which may indicate an osteocytic role in mineral homeostasis during hibernation. Osteocyte lacunar density and porosity were greater (+44 and +59%, respectively; P<0.0001) in hibernating compared with active squirrels, which may reflect a decrease in osteoblastic activity (per cell) during hibernation. Trabecular bone volume fraction in the proximal tibia was decreased (-20%; P0.028) in hibernating compared with physically active adult squirrels, but was not different between hibernating and active juvenile squirrels. Taken together, these data suggest that 13-lined ground squirrels may be unable to prevent microstructural losses of cortical and trabecular bone during hibernation, but importantly may possess a biological mechanism to preserve cortical bone macrostructure and strength during hibernation, thus preventing an increased risk of bone fracture during remobilization in the spring.

Renal adaptation during hibernation

“…Serum concentrations of phosphate and calcium tend to increase progressively and peak during late torpor but subsequently normalize during late arousal (101). The latter findings are consistent with the observation that smaller hibernators (such as the 13-lined ground squirrel) may excrete calcium liberated from bone during periodic arousals (72). In contrast, hibernating bears do not excrete waste, (72), remain eucalcemic throughout hibernation (102), and do not demonstrate bone loss, possibly because of lower bone turnover (119).…”

“…The latter findings are consistent with the observation that smaller hibernators (such as the 13-lined ground squirrel) may excrete calcium liberated from bone during periodic arousals (72). In contrast, hibernating bears do not excrete waste, (72), remain eucalcemic throughout hibernation (102), and do not demonstrate bone loss, possibly because of lower bone turnover (119). For further detailed information regarding bone metabolism the reader is referred to the excellent review by McGee-Lawrence et al (72).…”

“…In contrast, hibernating bears do not excrete waste, (72), remain eucalcemic throughout hibernation (102), and do not demonstrate bone loss, possibly because of lower bone turnover (119). For further detailed information regarding bone metabolism the reader is referred to the excellent review by McGee-Lawrence et al (72).…”

Prevention of muscle wasting and osteoporosis: the value of examining novel animal models

“…Although these studies lacked thorough quantification of a wide array of bone properties, for small mammalian hibernators there is still conflicting evidence as to whether bone loss regularly occurs during dormancy. Whereas both arctic and golden-mantled ground squirrels retain cortical bone properties and strength following hibernation (Utz et al, 2009;Wojda et al, 2012), data indicate that hibernating I. tridecemlineatus might be unable to avoid microstructural losses of cortical and trabecular bone (McGee-Lawrence et al, 2011). Nevertheless, because bone geometrical and mechanical properties do not differ significantly between hibernating and active squirrels, these animals can still perhaps activate the appropriate physiological mechanisms to maintain bone macrostructure and strength throughout hibernation in preparation for normal skeletal function during arousal.…”

Pre-suckling calcium supplementation effectively prevents lactation-induced osteopenia in rats

“…Osteocytes in the tibial cortical envelope could also contribute to calcium release from bone through a process known as osteocytic osteolysis (24,35). During the reproductive periods from late pregnancy (P21) to late lactation (L21), the osteocyte lacunar areas in tibiae were greater than those of the agematched nulliparous rats (Fig.…”