Effect of aestivation on long bone mechanical properties in the green-striped burrowing frog, Cyclorana alboguttata

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.

Section: Introductionsupporting

confidence: 74%

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

Utz

Nelson

O’Toole

et al. 2009

“…However, aestivation does not decrease bone strength or cross-sectional area in the long bones of green-striped burrowing frogs (Cyclorna alboguttata) (Hudson et al, 2004). After 9·months of aestivation there was no evidence of osteoclast activity; however, there was also no intracortical remodeling in nonaestivating frogs.…”

Section: Discussionmentioning

confidence: 89%

“…After 9·months of aestivation there was no evidence of osteoclast activity; however, there was also no intracortical remodeling in nonaestivating frogs. Unfortunately, little is known about the endocrinology of aestivating frogs (Hudson et al, 2004), and thus the mechanisms that preserve bone during aestivation are unknown.…”

Section: Discussionmentioning

confidence: 99%

Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis

Donahue

Galley

Vaughan

et al. 2006

SUMMARY Mechanical unloading of bone causes an imbalance in bone formation and resorption leading to bone loss and increased fracture risk. Black bears(Ursus americanus) are inactive for up to six months during hibernation, yet bone mineral content and strength do not decrease with disuse or aging. To test whether hibernating bears have biological mechanisms to prevent disuse osteoporosis, we measured the serum concentrations of hormones and growth factors involved in bone metabolism and correlated them with the serum concentration of a bone formation marker (osteocalcin). Serum was obtained from black bears over a 7-month duration that included periods of activity and inactivity. Both resorption and formation markers increased during hibernation, suggesting high bone turnover occurred during inactivity. However, bone formation appeared to be balanced with bone resorption. The serum concentration of parathyroid hormone (PTH) was higher in the hibernation(P=0.35) and post-hibernation (P=0.006) seasons relative to pre-hibernation levels. Serum leptin was lower (P<0.004)post-hibernation relative to pre-hibernation and hibernation periods. Insulin-like growth factor I (IGF-I) decreased (P<0.0001) during hibernation relative to pre-hibernation and reached its highest value during remobilization. There was no difference (P=0.64) in 25-OH vitamin D between the three seasons. Serum osteocalcin (bone formation marker) was significantly correlated with PTH, but not with leptin, IGF-I or 25-OH vitamin D. Osteocalcin and PTH were positively correlated when samples from all seasons were pooled and when only hibernation samples were considered, raising the possibility that the anabolic actions of PTH help maintain bone formation to prevent disuse osteoporosis. Prostaglandin E2 (PGE2)release from MC3T3 osteoblastic cells was significantly affected by treatment with bear serum from different seasons (i.e. hibernation versus active periods). The seasonal changes in PGE2 release showed trends similar to the seasonal changes in serum IGF-I. Since both PGE2 and IGF-I are associated with collagenous bone formation, it is possible that seasonal changes in a circulating factor influence IGF-I levels in vivo in bears and PGE2 release in osteoblastic cells in vitro. The significant decrease in serum leptin following arousal from hibernation may promote bone formation during remobilization, assuming there is a similar decrease in intracerebroventricular leptin. These findings support the idea that seasonal changes in the concentration of circulating molecules help regulate bone formation activity and may be important for preventing disuse osteoporosis in bears.

“…Consequently, the green-striped burrowing frog (C. alboguttata) has recently been used in our laboratory to study the effects of aestivation on skeletal muscle and bone, and the associated physiological and molecular processes that may confer resistance to musculoskeletal deterioration (Hudson et al, 2004(Hudson et al, , 2006Hudson and Franklin, 2002a;Mantle et al, 2009;Reilly et al, 2013;Symonds et al, 2007;Young et al, 2013). Prolonged inactivity associated with aestivation has been shown to have negligible effects on muscle mass, whole-muscle cross-sectional area, myofibre number, in vitro force production, bone-bending strength and swimming performance in C. alboguttata (Hudson et al, 2004(Hudson et al, , 2006Hudson and Franklin, 2002a;Mantle et al, 2009). The apparent absence of musculoskeletal losses in Cyclorana is consistent with the patterns reported for periods of disuse in hibernators as discussed above, and it is evident that the responses of muscle and bone to disuse in disparate organisms that undergo dormancy are profoundly different from those of typical models of disuse.…”

Section: Maintenance Of Musculoskeletal Properties In Hibernators Andmentioning

confidence: 99%

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

Reilly

Franklin

2016

Self Cite

Bone mass and skeletal muscle mass are controlled by factors such as genetics, diet and nutrition, growth factors and mechanical stimuli. Whereas increased mechanical loading of the musculoskeletal system stimulates an increase in the mass and strength of skeletal muscle and bone, reduced mechanical loading and disuse rapidly promote a decrease in musculoskeletal mass, strength and ultimately performance (i.e. muscle atrophy and osteoporosis). In stark contrast to artificially immobilised laboratory mammals, animals that experience natural, prolonged bouts of disuse and reduced mechanical loading, such as hibernating mammals and aestivating frogs, consistently exhibit limited or no change in musculoskeletal performance. What factors modulate skeletal muscle and bone mass, and what physiological and molecular mechanisms protect against losses of muscle and bone during dormancy and following arousal? Understanding the events that occur in different organisms that undergo natural periods of prolonged disuse and suffer negligible musculoskeletal deterioration could not only reveal novel regulatory factors but also might lead to new therapeutic options. Here, we review recent work from a diverse array of species that has revealed novel information regarding physiological and molecular mechanisms that dormant animals may use to conserve musculoskeletal mass despite prolonged inactivity. By highlighting some of the differences and similarities in musculoskeletal biology between vertebrates that experience disparate modes of dormancy, it is hoped that this Review will stimulate new insights and ideas for future studies regarding the regulation of atrophy and osteoporosis in both natural and clinical models of muscle and bone disuse.