Elsevier

Bone

Volume 145, April 2021, 115845
Bone

Osteoporosis prevention in an extraordinary hibernating bear

https://doi.org/10.1016/j.bone.2021.115845Get rights and content

Highlights

  • Hibernating bears have biological mechanisms to prevent disuse osteoporosis.

  • Black bears can resist disuse osteoporosis for up to 31 years.

  • Hibernating, physically inactive bears preserve bone by reducing bone remodeling.

  • Circulating factors may prevent osteocyte apoptosis in hibernating bears.

  • Circulating factors may prevent osteoclastic bone resorption in hibernating bears.

Abstract

Disuse osteoporosis results from physical inactivity. Reduced mechanical loading of bone stimulates bone resorption leading to bone loss, decreased mechanical properties, and increased fracture risk. Compensatory mechanisms evolved in hibernators to preserve skeletal muscle and bone during the prolonged physical inactivity that occurs during annual hibernation. This paper reports the preservation of bone properties in an exceptionally old black bear that was physically inactive for about 6 months annually for 31 years. The biological mechanisms that preserve bone during prolonged disuse during hibernation are also reviewed.

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.

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