Osteoporosis prevention in an extraordinary hibernating bear
Graphical abstract
Introduction
Physical inactivity leads to bone loss [1] and increased fracture risk [2]. However, bone has adapted to many extreme environmental conditions [3], which can provide insight for treating diseases [4,5]. For example, hibernating mammals mitigate muscle and bone atrophy during prolonged periods of physical inactivity that occur during hibernation [[6], [7], [8], [9], [10]]. Bears are physically inactive during hibernation which may last up to 6 months annually. For grizzly and black bears, aging and hibernation do not adversely affect the composition (e.g., mineral content), microstructure (e.g., intracortical porosity), or mechanical properties of cortical bone material [11,12] or whole bones [[13], [14], [15], [16]]. Trabecular bone mineral content and architecture are also preserved in hibernating bears [17]. Elucidating the biological mechanisms that preserves bone tissue in hibernators may lead to novel therapies for osteoporosis [18]. This paper reports the bone properties of an exceptionally long-lived black bear and discusses the current state of knowledge of the biological mechanisms that prevent disuse osteoporosis in hibernating bears.
Section snippets
Methods
Bone properties have previously been reported for black bears that were 1–19 years old [16,17]. It is rare for a bear to live past 20 years and rarer still for a bear to live past 30 years. In a study of 55,000 black bears, only 3 lived beyond the age of 30 years [19]. The black bear known as Xina was born in 1988, radio-collared in the Books Cliffs of Utah in 1992 at the age of 4, and died at the age of 31 in June of 2019. After being collared, she was visited in her hibernaculum every year
Results
Xina's bone cross-sectional geometrical properties at the midshaft of the femur were within the range of those measured for black bears previously (Table 1), albeit toward the low end of this range. This is not surprising given her low bodyweight at the time of her death. The strength and toughness of her femur were also within the range of values for younger bears. Femoral intracortical porosity and mineral content were also within the ranges of values reported previously (Fig. 1A and B).
Discussion
Bone is a mechanically responsive organ that demonstrates phenotypic plasticity in response to changing mechanical environments. However, bone is also an endocrine organ that plays important roles in reproduction and energy metabolism [20], and is essential for organismal calcium homeostasis [21]. Thus, there are many competing demands on the skeleton that influence bone remodeling. Hibernation is a mechanism to reduce metabolic energy expenditure overwinter when food is scarce [22,23]. Since
CRediT authorship contribution statement
Seth Donahue: wrote and revised the manuscript, data collection and analysis. Samantha Wojda: data collection. Meghan McGee-Lawrence: writing and methodology. Janene Auger: field data collection and writing. Hal Black: field data collection and writing.
References (49)
- et al.
Hibernating bears as a model for preventing disuse osteoporosis
J. Biomech.
(2006) - et al.
Bending properties, porosity, and ash fraction of black bear (Ursus americanus) cortical bone are not compromised with aging despite annual periods of disuse
J. Biomech.
(2004) - et al.
The tensile strength of black bear (Ursus americanus) cortical bone is not compromised with aging despite annual periods of hibernation
J. Biomech.
(2005) - et al.
Black bear femoral porosity decreases and mechanical properties increase with age despite annual periods of disuse (hibernation)
Eng. Fract. Mech.
(2007) - et al.
Decreased bone turnover with balanced resorption and formation prevent cortical bone loss during disuse (hibernation) in grizzly bears (Ursus arctos horribilis)
Bone.
(2008) - et al.
Six months of disuse during hibernation does not increase intracortical porosity or decrease cortical bone geometry, strength, or mineralization in black bear (Ursus americanus) femurs
J. Biomech.
(2009) - et al.
Grizzly bears (Ursus arctos horribilis) and black bears (Ursus americanus) prevent trabecular bone loss during disuse (hibernation)
Bone.
(2009) - et al.
Black bear parathyroid hormone has greater anabolic effects on trabecular bone in dystrophin-deficient mice than in wild type mice
Bone.
(2012) - et al.
Investigating the mechanism for maintaining eucalcemia despite immobility and anuria in the hibernating American black bear (Ursus americanus)
Bone.
(2011) - et al.
Interruption of disuse by short duration walking exercise does not prevent bone loss in the sheep calcaneus
Bone.
(1995)
Obesity is a concern for bone health with aging
Nutr. Res.
Long-term immobilization in elderly females causes a specific pattern of cortical bone and osteocyte deterioration different from postmenopausal osteoporosis
J. Bone Miner. Res.
Musculoskeletal morbidity following spinal cord injury: a longitudinal cohort study of privately-insured beneficiaries
Bone.
Evolutionary physiology of bone: bone metabolism in changing environments
Physiology.
Krogh’s principle for musculoskeletal physiology and pathology
J. Musculoskelet. Neuronal Interact.
Insights from the den: how hibernating bears may help us understand and treat human disease
Clin Transl Sci.
Calcium homeostasis during hibernation and in mechanical environments disrupting calcium homeostasis
J. Comp. Physiol. B.
Muscle strength in overwintering bears
Nature
Mammalian hibernation as a model of disuse osteoporosis: the effects of physical inactivity on bone metabolism, structure, and strength
Am. J. Phys. Regul. Integr. Comp. Phys.
Prevention of muscle wasting and osteoporosis: the value of examining novel animal models
J. Exp. Biol.
Black bear femoral geometry and cortical porosity are not adversely affected by ageing despite annual periods of disuse (hibernation)
J. Anat.
One very old bear
International Bear News
The contribution of bone to whole-organism physiology
Nature.
The physicochemical structure of bone: cellular and noncellular elements
Miner. Electrolyte Metab.
Cited by (3)
Bone adaptation and osteoporosis prevention in hibernating mammals
2023, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyInferring longevity from advanced rib remodelling in insular dwarf deer
2022, Biological Journal of the Linnean Society