ARTICLE IN PRESS
Journal of Biomechanics 39 (2006) 1480–1488
www.elsevier.com/locate/jbiomech
www.JBiomech.com
2004 American Society of Biomechanics Post-doctoral Young Scientist Award
Hibernating bears as a model for preventing disuse osteoporosis
Seth W. Donahuea,b,, Meghan E. McGeea, Kristin B. Harveyb,
Michael R. Vaughanc, Charles T. Robbinsd
a
Department of Biomedical Engineering, Michigan Technological University, 309 Minerals and Materials Engineering Building,
1400 Townsend Drive, Houghton, MI 49931, USA
b
Department of Mechanical Engineering—Engineering Mechanics, Michigan Technological University, Houghton, MI 49931, USA
c
US Geological Survey, Virginia Cooperative Fish and Wildlife Research Unit, Virginia Polytechnic Institute and State University,
Blacksburg, VA 24061-0321, USA
d
Department of Zoology, Washington State University, Pullman, WA 99164-4236, USA
Accepted 26 March 2005
Abstract
The hibernating bear is an excellent model for disuse osteoporosis in humans because it is a naturally occurring large animal
model. Furthermore, bears and humans have similar lower limb skeletal morphology, and bears walk plantigrade like humans.
Black bears (Ursus americanus) may not develop disuse osteoporosis during long periods of disuse (i.e. hibernation) because they
maintain osteoblastic bone formation during hibernation. As a consequence, bone volume, mineral content, porosity, and strength
are not adversely affected by annual periods of disuse. In fact, cortical bone bending strength has been shown to increase with age in
hibernating black bears without a significant change in porosity. Other animals require remobilization periods 2–3 times longer than
the immobilization period to recover the bone lost during disuse. Our findings support the hypothesis that black bears, which
hibernate for as long as 5–7 months annually, have evolved biological mechanisms to mitigate the adverse effects of disuse on bone
porosity and strength.
r 2005 Elsevier Ltd. All rights reserved.
Keywords: Disuse osteoporosis; Bone mechanical properties; Bone remodeling; Black bear; Aging; Hibernation
1. Introduction
We have collected some evidence to support the
hypothesis that black bears (Ursus americanus) have
evolved biological mechanisms to mitigate or avoid the
adverse effects of disuse on bone and/or have better
compensatory mechanisms to more rapidly recover from
disuse osteoporosis.
Others have provided additional evidence to support
this hypothesis (Floyd et al., 1990; Pardy et al., 2004).
Corresponding author. Department of Biomedical Engineering,
Michigan Technological University, 309 Minerals and Materials
Engineering Building, 1400 Townsend Drive, Houghton, MI 49931,
USA. Tel.: +1 906 487 1729; fax: +1 906 487 1717.
E-mail address: [email protected] (S.W. Donahue).
0021-9290/$ - see front matter r 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jbiomech.2005.03.030
The hibernating black bear is an excellent model for
disuse osteoporosis in humans because it is a naturally
occurring large animal model. Furthermore, black
bears and humans have similar lower limb skeletal
morphology and bears walk plantigrade like humans.
We have quantified age-related changes in the material
properties, histology, mineral content, and whole
bone bending strength of black bear cortical bone.
We have used this data to make inferences about how
bear bones are affected by disuse. The inferences
we have made are based on the fact that other
species require remobilization periods of 2–3 times the
length of the disuse period to recover lost bone (Kaneps
et al., 1997; Weinreb et al., 1997). In a study on
long-term immobilization in dogs, 32 weeks of disuse
resulted in significant relative bone loss in both young
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and old dogs (Jaworski and Uhthoff, 1986). After 28
weeks of remobilization, young dogs recovered
only 70% of the cortical bone lost during disuse and
old dogs recovered only 40% of the lost cortical bone.
These findings suggest that black bears, which hibernate
for 5–6 months annually in northern regions (e.g.,
Michigan), should not have a sufficient recovery
period to regain bone if they lose it at the same rate as
dogs. We are trying to answer some important questions
regarding hibernating bears: (1) if bears do lose bone
during disuse, how can they recover sufficient bone
when their active and disuse (i.e., hibernation) periods
are approximately equal in duration and (2) if they are
able to prevent or mitigate bone loss during disuse, what
are the biological mechanisms? The purpose of this
paper is to summarize the observations on bone
metabolism and mechanics in hibernating bears and
start to piece together a theory on how bone mass and
strength are regulated by bears during lengthy periods
of inactivity.
Disuse osteoporosis occurs in patients with spinal
cord injuries, patients confined to prolonged bed rest,
and astronauts exposed to microgravity during
spaceflight (Leblanc et al., 1990; Garland et al., 1992;
Collet et al., 1997; Dauty et al., 2000; Vico et al., 2000).
During remobilization, the recovery of the bone lost
during disuse is slow and may not be complete
(Lindgren and Mattsson, 1977; Jaworski and Uhthoff,
1986; Leblanc et al., 1990; Vico et al., 2000). In fact,
bone loss can continue during remobilization (Trebacz,
2001). Animal studies have shown that immediate rapid
increases in bone resorption and sustained decreases in
bone formation contribute to bone loss during limb
immobilization by casting, tenotomy, or neurectomy
(Weinreb et al., 1989; Rantakokko et al., 1999).
Following 2 weeks of hind limb immobilization
and 4 weeks of remobilization, the bending strength,
apparent density, and degree of mineralization of rat
femurs were significantly lower than in age-matched
controls (Trebacz, 2001). In other studies where
remobilization did restore the bone lost by immobilization, the recovery period was 2–3 times longer than the
immobilization period (Kaneps et al., 1997; Weinreb
et al., 1997). In hibernating ground squirrels, golden
hamsters, and little brown bats bone is lost by reduced
bone formation and increased bone resorption
(Haller and Zimny, 1977; Steinberg et al., 1979;
Steinberg et al., 1981; Steinberg et al., 1986; Kwiecinski
et al., 1987). In black bears both bone resorption
and formation surfaces increase in trabecular bone
during hibernation relative to summer (Floyd et al.,
1990), although bone mineral density and content,
bone volume fraction, and trabecular thickness are
not significantly different in the autumn (prior to
hibernation) and spring (following hibernation) (Pardy
et al., 2004).
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2. What level of disuse do bears experience during
hibernation?
Many animals hibernate in response to seasonal
variations in food supplies, including bears which
remain dormant for 3–7 months. Many hibernators
periodically wake (every 4–10 days) to eat, urinate, and
defecate; black bears do not. Black bear resting heart
rate drops from 40 beats per minute to as low as 8 beats
per minute during hibernation (Hellgren, 1998). Black
bear body temperature only drops a few degrees Celsius
during hibernation; however, the body temperature of
other hibernators can drop below freezing (Harlow et
al., 2004). Hibernating bears lose as much as 37% of
their bodyweight during hibernation, primarily by the
catabolism of fat stores (Hellgren, 1998). There is a
significant decrease in skeletal muscle protein concentration during hibernation, although muscle crosssectional area does not change (Tinker et al., 1998).
Black bear muscle strength significantly decreases (23%)
during hibernation (Harlow et al., 2001). However, this
level of strength loss is much less than what was
predicted to occur in humans for a disuse period
equivalent in duration to hibernation. Bone formation,
bone volume, and bone mineral content do not decrease
during this period of inactivity (Floyd et al., 1990;
Donahue et al., 2003a; Pardy et al., 2004). Clearly
hibernating bears have evolved some unique biological
mechanisms to survive long periods of limited food
supplies and inactivity.
The captive black bears we have studied den in 4-foot
diameter, 6-foot long culverts filled with straw. They are
essentially inactive during the denning period. They
have not been observed leaving the den although they do
rearrange the straw to some extent. Wild black bears in
Minnesota typically hibernate in dens too small to
permit standing and do not leave the den over the course
of hibernation (Rogers, 2004). The wild bears we have
studied in Virginia hibernate for 4–4.5 months; most of
them tightly fit into hollow trees. Thus, in many
instances, if bears mechanically load their bones during
hibernation they would have to do so by shivering or
non-standing exercise (perhaps isometric muscle contractions). Shivering has been observed in black bears
hibernating in northern Minnesota, using infrared
cameras (Rogers, 2004). Harlow et al. (2004) suggested
that bears use 3–4 daily bouts of skeletal muscle activity
to mitigate muscle strength loss (Harlow et al., 2004).
Pardy et al. (2004) suggested that skeletal muscle
shivering in bears may be sufficient to maintain
trabecular bone mass and microarchitecture by a
mechanism involving low magnitude, high-frequency
mechanical stimulation, because daily 10 min bouts of
low magnitude, high-frequency mechanical stimulation
prevented disuse-induced decreases in bone formation
rate in hind limb suspended rats (Rubin et al., 2001).
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However, the high-frequency stimulation was superimposed on the rats normal weight bearing activities;
wild bears shiver while laying down because most dens
are too small to permit standing (Rogers, 2004).
Furthermore, high frequency, low magnitude (e.g., 5
microstrain) mechanical stimuli are only anabolic for
trabecular bone, not cortical bone (Rubin et al., 2002),
and our findings suggest that black bear cortical bone is
not impaired by disuse (Donahue and Harvey, 2004;
Harvey and Donahue, 2004; McGee et al., 2004).
During hibernation, captive grizzly bears also show
short bouts (o0.2 s) of local muscle shuddering activity
with episodes of periodic activation (3–10 s between
bouts) lasting longer than an hour (Lin et al., 2004).
Shuddering is described as less vigorous than shivering.
It is unclear if shivering can provide sufficient mechanical stimulation to maintain bone mass in hibernating
bears. Shivering is probably used to raise body
temperature in response to decreasing ambient temperatures and not a mechanism to maintain bone mass, since
more frequent shivering in hibernating bears is associated with colder ambient temperatures (Barnes, 2004).
We recently began studies on bone remodeling and
mechanics in hibernating grizzly bears (Ursus arctos
horribilis). Captive grizzly bears used in these studies
hibernate in 3 m square concrete dens and have free
access to 3 6 m outside runs. However, they are active
for less than 20 min per day during hibernation. Females
that gave birth averaged only 2.5 min of activity per day
during the first 6 weeks of lactation. Otherwise, they
were lay continuously while caring for and nursing the
cubs. It is important to note that these captive bears are
well fed during their active period and may not need to
conserve as much energy during hibernation as wild
bears as they are frequently fatter than wild bears.
Hibernation is a survival response to food shortages,
thus it would be counter-productive to survival to burn
calories for exercise during hibernation to maintain
muscle and bone strength. Even 20 min of daily activity
in captive grizzlies represents a considerable reduction in
activity level during hibernation; during the summer
these bears are active (i. e., traveling and foraging) for
about 15.2 h per day (Rode et al., 2001).
There is likely some low level of mechanical stimulation (e.g., due to shivering, rolling over, or grooming in
the den) on the bones of hibernating bears (i.e., they are
not in a complete state of disuse). But, is this level of
mechanical stimulation sufficient to maintain bone
mass? Astronauts lose significant bone mass in microgravity (i. e., during spaceflight) despite rigorous
musculoskeletal conditioning exercises (Lang et al.,
2004). Femoral neck bending strength index decreased
2.55%/month for spaceflights lasting 4–6 months (Lang
et al., 2004). This was associated with endosteal
expansion without periosteal apposition. Daily bouts
of exercise (up to 1.5 h) were unable to prevent, and in
some cases exacerbated, disuse-induced cortical thinning
and mechanical property loss in rat tibiae and femora
(Shaw et al., 1987). Given the results of studies on
humans and other animals and the low levels of activity
in hibernating bears, it seems likely that there are
biological factors that regulate bone metabolism, mass,
and strength in hibernating bears, either alone or in
combination with low-level mechanical factors.
3. Serum markers of bone metabolism in hibernating
bears
We have collected blood from captive and wild
hibernating black bears in almost every month of the
year. The serum was assayed for biochemical markers
(i.e, type I collagen peptides) of bone resorption and
bone formation. During bone formation, the carboxyterminal propeptide of type I procollagen (PICP) is
cleaved off and released into the circulation. The
concentration of PICP in serum has been positively
correlated with histomorphometric measurements of
bone formation (Eriksen et al., 1993). During resorption
of bone, cross-linked carboxy-terminal telopeptide
(ICTP) fragments are released into the circulation.
Serum ICTP has been positively correlated with bone
resorption and negatively correlated with bone mineral
density (Eriksen et al., 1993; Yasumizu et al., 1998). Our
data on hibernating black bears suggest that bone
resorption increases during disuse (Donahue et al.,
2003b; Donahue et al., 2003a). This was expected
since increased bone resorption is a common feature
of disuse in many animals. However, probably our most
500
b
400
PICP (µg/L)
1482
300
a
a
200
100
0
pre-hibernation
hibernation
post-hibernation
Fig. 1. Mean serum PICP concentrations for the three study periods.
Data are shown as mean value bar plots with standard error bars.
Groups with the same letter are not significantly (po0:05) different
from each other. The PICP concentration was not significantly
different during hibernation than during the pre-hibernation period.
However, post-hibernation, PICP concentration was significantly
higher than in the other two periods. Originally appeared in Donahue
et al. (2003a).
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interesting finding is that the serum marker of bone
formation did not decrease during disuse. This is
contrary to other animal studies which show decreased
bone formation during disuse (Dehority et al., 1999;
Rubin et al., 2001). In both our studies we found that
the mean formation marker levels (averaged over an
entire period) were not significantly different between
the pre-hibernation and hibernation periods, but significantly increased during the remobilization period
(Fig. 1). In our time-course study of these markers in
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captive bears the formation marker actually increased
shortly after the onset of disuse (Fig. 2B), possibly to
maintain the normal balance between bone resorption
(Fig. 2A) and formation (Donahue et al., 2003a). This
finding supports the histological data of Floyd et al.
(1990), which showed increased bone resorption and
formation surfaces during hibernation. In both our wild
and captive bear studies, the formation marker was
significantly increased immediately upon remobilization
(Donahue et al., 2003b; Donahue et al., 2003a).
40
ICTP (µg/L)
30
20
10
arousal
hibernation
0
10/1/2001
10/31/2001
11/30/2001
(A)
12/30/2001
1/29/2002
2/28/2002
3/30/2002
Sample Date
500
PICP (µg/L)
400
300
200
100
arousal
hibernation
0
10/1/2001
(B)
10/31/2001
11/30/2001
12/30/2001
1/29/2002
2/28/2002
3/30/2002
Sample date
Fig. 2. (A) Seasonal variations in the serum concentration of the bone resorption marker ICTP; mean values (n ¼ 5) with standard error bars. The
arrows indicate the beginning and ending of hibernation. (B) Seasonal variations in the serum concentration of the bone formation marker PICP.
Bone formation increased shortly after the onset of hibernation, possibly to maintain balance with the increase in resorption that occurs during
hibernation. Originally appeared in Donahue et al. (2003a).
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Human
Black Bear
400
Ultimate Stress (MPa)
Two possible interpretations for our data are that (1)
bone is not lost during disuse because bone formation
remains coupled to bone resorption even though the rate
of turnover increases, or (2) some bone is lost during
disuse because the increase in resorption is greater than
the increase in formation, but the bone lost during
disuse is rapidly recovered during remobilization following spring arousal. A possible explanation for the
former interpretation is that bone resorption increases
during disuse because of the lack of mechanical
stimulation, but because bears do not urinate or
defecate during hibernation and blood calcium concentrations remain stable (Floyd et al., 1990), bone
formation may increase to prevent blood calcium
concentration from becoming too high. Thus, the
calcium regulatory hormones may help regulate osteoblastic activity to retain a normal balance between
resorption and formation. An explanation for the later
is that there is some bone loss during disuse because
there is an imbalance between resorption and formation
(i.e., the increase in resorption is greater than the
increase in formation), but during disuse the bone cells
become accustomed to perceiving very low or absent
levels of mechanical stimulation as normal, so that when
mechanical loading resumes during remobilization the
bone cells perceive the mechanical loading level as high
and activate a bone formation response, in accordance
with mechanostat theory (Frost, 1987), to rapidly
recover the bone lost during disuse. Interestingly,
MC3T3 osteoblastic cells cultured in black bear serum,
show PGE2 levels with a seasonal pattern strikingly
similar to the seasonal changes in the bone formation
marker PICP (Fig. 1) (Donahue et al., 2004). Since
PGE2 is a potent stimulator of bone formation in vivo
(Jee and Ma, 1997), our findings suggest that seasonal
variations in the concentrations of circulating molecules
help regulate bone formation.
Black Bear
350
p = 0.008
300
r2 = 0.456
250
200
150
100
Human
50
p = 0.0001
r2 = 0.6194
0
0.0
0.1
0.2
0.3
0.4
Age/ Life Span
0.5
0.6
0.7
Fig. 3. The bending strength of cortical bone coupons from black bear
tibias significantly increased with age. The same trend was found for
human cortical bone by Currey and Butler (1975) for the same relative
age group. Originally published in Harvey and Donahue (2004).
Human
Black Bear
0.70
Black Bear
p = 0.0247
0.68
r2 = 0.311
Ash Fraction
1484
0.66
0.64
0.62
Human
p < 0.0001
r2 = 0.666
0.60
0.58
0.0
0.1
0.2
0.3
0.4
Age/ Life Span
0.5
0.6
0.7
Fig. 4. Cortical bone ash fraction significantly increased with age in
black bear tibias, as it did in human cortical bone for the same relative
age group (Currey and Butler, 1975). Originally published in Harvey
and Donahue (2004).
4. Age-related changes in bone strength
To assess the effects of annual periods of disuse on
bone mechanical behavior we have tested cortical bone
coupons, machined from black bear tibial diahpyses, in
uniaxial tension and three-point bending. We have also
loaded whole black bear tibias to failure in three-point
bending. Tibiae were obtained from black bears that
were killed late in their active period (September–October) by licensed hunters in the Upper Peninsula of
Michigan. The ages of the bears were determined, by the
Michigan Department of Natural Resources, from the
dental growth layers in the teeth (Coy and Garshelis,
1992). Sex differences in bone strength (i.e., ultimate
stress) were assessed using ANCOVA treating age as the
covariant. There were no significant (p ¼ 0:38) differences between males and females, therefore the data
were pooled and regressed against age. The ultimate
stress significantly (p ¼ 0:008) increased with age for
cortical bone coupons loaded in three-point bending
(Fig. 3) (Harvey and Donahue, 2004). The rate of
increase was similar to that of human cortical bone for
the same relative age ranges (i.e., growth–maturity),
although bear bone was stronger than human bone
(Currey and Butler, 1975). The age-related increases in
strength were probably due in part to age-related
increases in mineral content (Fig. 4). Notably, black
bear cortical bone porosity showed a trend towards an
age-related decrease (Fig. 5), which contrasts the agerelated increase in human bone porosity (Wang and Ni,
2003). These data are exceptional when one considers
that these bears were inactive for 5–6 months every year,
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and other animals lose significant bone mass during
disuse and require recovery periods 2–3 times longer
than the disuse period to recover the lost bone (Kaneps
et al., 1997; Weinreb et al., 1997). Yet, black bears are
able to increase bone strength at approximately the
same rate as humans. We have also found that for whole
bone bending, the ultimate stress did not significantly
change with age, although the results approached a
significant (p ¼ 0:051) age-related increase in strength
(McGee et al., 2004). Cortical bone tensile strength did
not significantly (p ¼ 0:16) change with age (Donahue
and Harvey, 2004). Taken together our findings suggest
that either (1) cortical bone strength is not adversely
affected by disuse (possibly because osteoblastic activity
and bone formation are not impaired by disuse), or (2)
bears are able to recover bone lost during disuse much
faster than other animals; serum markers of bone
Black Bear
Human
12
Human
10
p = 0.0001
Porosity (%)
r2 = 0.685
8
6
4
Black Bear
2
p = 0.1145
0
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
Age/ Life Span
Fig. 5. The porosity of black bear cortical bone did not change with
age, but increased in humans for the same relative age group (Wang
and Ni, 2003). Originally published in Harvey and Donahue (2004).
1485
formation are significantly elevated during remobilization immediately after hibernation (Donahue et al.,
2003b; Donahue et al., 2003a).
5. Histological and cross-sectional properties during
hibernation
Osteopenia results from decreased osteoblastic formation and increased osteoclastic resorption, decreasing
the total amount of bone in the skeleton after a
prolonged period of disuse (Weinreb et al., 1989;
Rantakokko et al., 1999). In a study on long-term
immobilization in dogs, 32 weeks of disuse resulted in
significant relative bone loss in both young and old dogs
(Jaworski and Uhthoff, 1986). Bone loss was manifest as
increased intracortical porosity and decreased cortex
thickness. When turkey ulnar diaphyses were in a state
of disuse for 4 weeks there was a significant decrease in
cross-sectional area and a significant increase (4-fold) in
intracortical pore size (Rubin et al., 1996). We recently
measured intracortical pore areas in tibias from a 9month old active grizzly bear and a 13-month old that
had been hibernating for 17 weeks. The resorption
cavity area was larger (1.7-fold) during hibernation, but
not to the extent of the increase observed in other
animals during disuse (i.e., 4-fold) (Rubin et al., 1996).
However, there were fewer resorption cavities during
hibernation, suggesting that intracortical porosity might
not change, or even decrease, during hibernation
(Fig. 6). Obviously these histological measures need to
be more thoroughly investigated before any conclusions
can be drawn, but our preliminary observations support
Fig. 6. Anterior cortices from the midshaft of the tibia from (A) an active 9-month old grizzly bear, and (B) a 13-month old grizzly bear 17 weeks
into hibernation. Intracortical porosity does not appear to increase during hibernation.
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Table 1
Observations on bone remodeling, histology, mechanical behavior, and biology from studies on hibernating black bears
Observation
Possible explanation
Bone resorption and formation surfaces, and bone formation rate
increase 3-4 fold during hibernation relative to summer with no change
in bone volume (Floyd et al., 1990).
Resorption increases due to a lack of mechanical stimulation in
accordance with mechanostat theory. Because bears do not urinate or
defecate during hibernation and blood calcium concentration remains
constant, calcium regulatory hormones (and possibly other hormones
and growth factors) help maintain bone formation and bone mass.
Serum markers of bone resorption and formation indicate increased
bone resorption during hibernation, and an increase or no change in
bone formation (Donahue et al., 2003a,b).
During remobilization in the spring, the bone formation rate increases
7-fold over the hibernation value and bone resorption surface decreases
(Floyd et al., 1990).
During remobilization, the bone formation marker increases several
fold and the resorption marker returns to pre-hibernation values
(Donahue et al., 2003a,b).
There is a possible imbalance between resorption and formation during
hibernation, even though both may be increased, resulting in a net bone
loss. During hibernation bone cells may become accustomed to
perceiving very low or absent levels of mechanical stimulation as
normal, so that when mechanical loading resumes they perceive the
mechanical loading level as high and activate a bone formation
response.
Trabecular bone mineral density and content, volume fraction,
structural model index, and trabecular thickness are not significantly
different in black bears killed in the spring compared to black bears
killed in the autumn (Pardy et al., 2004).
This suggests that bone resorption and formation are balanced during
hibernation such that there is no net trabecular bone loss in the ulna
and radius. It should be noted that the serum markers of bone turnover
reflect cortical and trabecular bone turnover in the entire skeleton.
Cortical bone bending strength, stiffness, and ash fraction significantly
increase with age and porosity is unchanged (Harvey and Donahue,
2004).
The ability to maintain bone formation during disuse and/or rapidly
increase bone formation upon remobilization allows bear to increase
bone strength with aging despite annual 6-month periods of disuse.
Other species require remobilization periods 2–3 times longer than the
disuse period to recover bone strength.
The ultimate stress in whole tibiae loaded in three-point bending shows
a trend of increasing with age (McGee et al., 2004).
Black bear serum modulates PGE2 release in MC-3T3 osteoblastic cells
with the same seasonal variation as the serum concentration of the
bone formation marker PICP (Donahue et al., 2004).
This suggest that the serum molecules which regulate bone formation in
vivo also regulate the release of a molecule (PGE2), associated with
bone formation, from bone cells in vitro.
Possible explanations for the observed phenomena are given in attempt to synthesize the data and form a theory on the regulation of bone mass and
strength in hibernating bears.
the theory that hibernating bears do not develop disuse
osteoporosis.
6. Summary
The existing evidence suggests that hibernating bears
do not develop disuse osteoporosis. The evidence is
summarized in Table 1 in an attempt to formulate a
theory on how bears resist disuse-induced bone loss.
Bone mineral density and content, bone volume fraction, and trabecular thickness are not significantly
affected by hibernation (Pardy et al., 2004), probably
because bone formation is not impaired by disuse
(Floyd et al., 1990; Donahue et al., 2003a,b). As a
consequence, bone strength is not adversely affected by
annual periods of disuse (Donahue and Harvey, 2004;
Harvey and Donahue, 2004; McGee et al., 2004). In
fact, cortical bone bending strength has been shown to
increase with age in hibernating black bears without a
significant change in porosity (Harvey and Donahue,
2004). The level of activity exhibited by bears during
hibernation is considerably less than what they exhibit
during the summer and should not be sufficient to
maintain bone formation, mass, and strength by itself.
We hypothesize that seasonal changes in the concentrations of circulating molecules (e.g., hormones), in the
absence of calcium excretion, are central to preserving
bone formation, mass, and strength during disuse. It is
likely that many molecules act in concert, and possibly
interact with the low levels of mechanical stimulation (e.
g., shivering) experienced during hibernation. Clearly
much is yet to be learned about the biological
mechanisms that regulate bone metabolism in hibernating bears. We are optimistic that understanding these
mechanisms will contribute to the development of
anabolic therapies for osteoporosis in humans.
Acknowledgments
Funding from the National Institutes of Health
(NIAMS AR050420), NASA and the Michigan Space
Grant Consortium, and Timothy Floyd, MD. Doug
Wagner from the Michigan Department of Natural
Resources allowed us to collect bones from hunter-killed
bears.
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