{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T12:29:39Z","timestamp":1790512179395,"version":"4.1.0"},"reference-count":41,"publisher":"The Company of Biologists","issue":"13","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,7,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Decreased physical activity in mammals increases bone turnover and uncouples bone formation from bone resorption, leading to hypercalcemia, hypercalcuria, bone loss and increased fracture risk. Black bears, however, are physically inactive for up to 6\u2005months annually during hibernation without losing cortical or trabecular bone mass. Bears have been shown to preserve trabecular bone volume and architectural parameters and cortical bone strength, porosity and geometrical properties during hibernation. The mechanisms that prevent disuse osteoporosis in bears are unclear as previous studies using histological and serum markers of bone remodeling show conflicting results. However, previous studies used serum markers of bone remodeling that are known to accumulate with decreased renal function, which bears have during hibernation. Therefore, we measured serum bone remodeling markers (BSALP and TRACP) that do not accumulate with decreased renal function, in addition to the concentrations of serum calcium and hormones involved in regulating bone remodeling in hibernating and active bears. Bone resorption and formation markers were decreased during hibernation compared with when bears were physically active, and these findings were supported by histomorphometric analyses of bone biopsies. The serum concentration of cocaine and amphetamine regulated transcript (CART), a hormone known to reduce bone resorption, was 15-fold higher during hibernation. Serum calcium concentration was unchanged between hibernation and non-hibernation seasons. Suppressed and balanced bone resorption and formation in hibernating bears contributes to energy conservation, eucalcemia and the preservation of bone mass and strength, allowing bears to survive prolonged periods of extreme environmental conditions, nutritional deprivation and anuria.<\/jats:p>","DOI":"10.1242\/jeb.120725","type":"journal-article","created":{"date-parts":[[2015,7,8]],"date-time":"2015-07-08T17:20:18Z","timestamp":1436376018000},"page":"2067-2074","source":"Crossref","is-referenced-by-count":52,"title":["Suppressed bone remodeling in black bears conserves energy and bone mass during hibernation"],"prefix":"10.1242","volume":"218","author":[{"given":"Meghan","family":"McGee-Lawrence","sequence":"first","affiliation":[{"name":"Department of Cellular Biology and Anatomy, Georgia Regents University, Augusta, GA 30912, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia","family":"Buckendahl","sequence":"additional","affiliation":[{"name":"Center for Alcohol Studies, Rutgers University, New Brunswick, NJ 08901, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caren","family":"Carpenter","sequence":"additional","affiliation":[{"name":"Department of Orthopaedics and Rehabilitation, Yale University, New Haven, CT 06520, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kim","family":"Henriksen","sequence":"additional","affiliation":[{"name":"Nordic Bioscience Biomarkers and Research, Herlev, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Vaughan","sequence":"additional","affiliation":[{"name":"Department of Fish and Wildlife Conservation, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seth","family":"Donahue","sequence":"additional","affiliation":[{"name":"Department of Mechanical Engineering, Colorado State University, Fort Collins, CO 80523, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042508445765100_JEB120725C1","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1038\/nrendo.2012.201","article-title":"The role of osteocalcin in human glucose metabolism: marker or mediator?","volume":"9","author":"Booth","year":"2013","journal-title":"Nat. Rev. Endocrinol."},{"key":"2021042508445765100_JEB120725C2","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1152\/ajplegacy.1971.220.1.293","article-title":"Renal function in anesthetized dormant and active bears","volume":"220","author":"Brown","year":"1971","journal-title":"Am. J. Physiol."},{"key":"2021042508445765100_JEB120725C3","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1210\/er.17.4.333","article-title":"Molecular basis and clinical application of biological markers of bone turnover","volume":"17","author":"Calvo","year":"1996","journal-title":"Endocr. Rev."},{"key":"2021042508445765100_JEB120725C4","doi-asserted-by":"publisher","first-page":"1153","DOI":"10.1152\/physrev.00008.2003","article-title":"Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature","volume":"83","author":"Carey","year":"2003","journal-title":"Physiol. Rev."},{"key":"2021042508445765100_JEB120725C5","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.ymgme.2014.09.003","article-title":"Role of adiponectin system in insulin resistance","volume":"113","author":"Caselli","year":"2014","journal-title":"Mol. Genet. Metab."},{"key":"2021042508445765100_JEB120725C41","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1152\/physiol.00022.2014","article-title":"Evolutionary physiology of bone: bone metabolism in changing environments","volume":"30","author":"Doherty","year":"2015","journal-title":"Physiology"},{"key":"2021042508445765100_JEB120725C6","doi-asserted-by":"publisher","first-page":"1630","DOI":"10.1242\/jeb.02185","article-title":"Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis","volume":"209","author":"Donahue","year":"2006","journal-title":"J. Exp. Biol."},{"key":"2021042508445765100_JEB120725C7","doi-asserted-by":"publisher","first-page":"1850","DOI":"10.1359\/jbmr.080610","article-title":"Bone markers predict cardiovascular events in chronic kidney disease","volume":"23","author":"Fahrleitner-Pammer","year":"2008","journal-title":"J. Bone Miner. Res."},{"key":"2021042508445765100_JEB120725C8","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1097\/00003086-199006000-00041","article-title":"Calcium and bone metabolic homeostasis in active and denning black bears (Ursus americanus)","volume":"255","author":"Floyd","year":"1990","journal-title":"Clin. Orthop."},{"key":"2021042508445765100_JEB120725C9","first-page":"7","article-title":"The physicochemical structure of bone: cellular and noncellular elements","volume":"20","author":"Green","year":"1994","journal-title":"Miner. Electrolyte Metab."},{"key":"2021042508445765100_JEB120725C10","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1002\/jor.1100130510","article-title":"Uniformity of resorptive bone loss induced by disuse","volume":"13","author":"Gross","year":"1995","journal-title":"J. Orthop. Res."},{"key":"2021042508445765100_JEB120725C11","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1038\/35059165","article-title":"Muscle strength in overwintering bears","volume":"409","author":"Harlow","year":"2001","journal-title":"Nature"},{"key":"2021042508445765100_JEB120725C12","first-page":"467","article-title":"Physiology of hibernation in bears","volume":"10","author":"Hellgren","year":"1998","journal-title":"Ursus"},{"key":"2021042508445765100_JEB120725C13","doi-asserted-by":"publisher","first-page":"291","DOI":"10.2307\/1381939","article-title":"Serial changes in metabolic correlates of hibernation in female black bears","volume":"71","author":"Hellgren","year":"1990","journal-title":"J. Mammal."},{"key":"2021042508445765100_JEB120725C14","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1007\/s00198-006-0286-8","article-title":"Assessment of osteoclast number and function: application in the development of new and improved treatment modalities for bone diseases","volume":"18","author":"Henriksen","year":"2007","journal-title":"Osteoporos. Int."},{"key":"2021042508445765100_JEB120725C15","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1038\/nature10763","article-title":"The contribution of bone to whole-organism physiology","volume":"481","author":"Karsenty","year":"2012","journal-title":"Nature"},{"key":"2021042508445765100_JEB120725C16","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1007\/s11914-013-0157-0","article-title":"Influence of hormonal appetite and energy regulators on bone","volume":"11","author":"Khor","year":"2013","journal-title":"Curr. Osteoporos. Rep."},{"key":"2021042508445765100_JEB120725C17","doi-asserted-by":"publisher","first-page":"301S","DOI":"10.1016\/8756-3282(94)00045-2","article-title":"Calcium absorption, endogenous excretion, and endocrine changes during and after long-term bed rest","volume":"16","author":"LeBlanc","year":"1995","journal-title":"Bone"},{"key":"2021042508445765100_JEB120725C18","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.tem.2008.02.006","article-title":"Reciprocal regulation of bone and energy metabolism","volume":"19","author":"Lee","year":"2008","journal-title":"Trends Endocrinol. Metab."},{"key":"2021042508445765100_JEB120725C19","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1359\/JBMR.041010","article-title":"Long-term disuse osteoporosis seems less sensitive to bisphosphonate treatment than other osteoporosis","volume":"20","author":"Li","year":"2005","journal-title":"J. Bone Miner. Res."},{"key":"2021042508445765100_JEB120725C20","doi-asserted-by":"publisher","first-page":"756","DOI":"10.1016\/j.bone.2012.07.001","article-title":"Effect of proton irradiation followed by hindlimb unloading on bone in mature mice: a model of long-duration spaceflight","volume":"51","author":"Lloyd","year":"2012","journal-title":"Bone"},{"key":"2021042508445765100_JEB120725C21","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1016\/j.bone.2007.10.010","article-title":"Decreased bone turnover with balanced resorption and formation prevent cortical bone loss during disuse (hibernation) in grizzly bears (Ursus arctos horribilis)","volume":"42","author":"McGee","year":"2008","journal-title":"Bone"},{"key":"2021042508445765100_JEB120725C22","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.1016\/j.jbiomech.2008.11.039","article-title":"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","volume":"42","author":"McGee-Lawrence","year":"2009","journal-title":"J. Biomech."},{"key":"2021042508445765100_JEB120725C23","doi-asserted-by":"publisher","first-page":"1186","DOI":"10.1016\/j.bone.2009.08.011","article-title":"Grizzly bears (Ursus arctos horribilis) and black bears (Ursus americanus) prevent trabecular bone loss during disuse (hibernation)","volume":"45","author":"McGee-Lawrence","year":"2009","journal-title":"Bone"},{"key":"2021042508445765100_JEB120725C24","doi-asserted-by":"publisher","first-page":"850","DOI":"10.1016\/S0025-6196(12)62341-6","article-title":"Black bears and polar bears\u2014still metabolic marvels","volume":"62","author":"Nelson","year":"1987","journal-title":"Mayo Clin. Proc."},{"key":"2021042508445765100_JEB120725C25","first-page":"141","article-title":"Nitrogen metabolism in bears: urea metabolism in summer starvation and in winter sleep and role of urinary bladder in water and nitrogen conservation","volume":"50","author":"Nelson","year":"1975","journal-title":"Mayo Clin. Proc."},{"key":"2021042508445765100_JEB120725C26","first-page":"137","article-title":"Neuroendocrine and metabolic interactions in the hibernating black bear","volume":"174","author":"Nelson","year":"1983","journal-title":"Acta Zool. Fennica."},{"key":"2021042508445765100_JEB120725C27","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1126\/science.6494914","article-title":"Ratio of serum urea to serum creatinine in wild black bears","volume":"226","author":"Nelson","year":"1984","journal-title":"Science"},{"key":"2021042508445765100_JEB120725C28","doi-asserted-by":"publisher","first-page":"1170","DOI":"10.2460\/javma.2003.223.1170","article-title":"Evaluation of cardiac function in active and hibernating grizzly bears","volume":"223","author":"Nelson","year":"2003","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"2021042508445765100_JEB120725C29","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1016\/j.cmet.2014.07.008","article-title":"Grizzly bears exhibit augmented insulin sensitivity while obese prior to a reversible insulin resistance during hibernation","volume":"20","author":"Nelson","year":"2014","journal-title":"Cell Metab."},{"key":"2021042508445765100_JEB120725C30","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1079\/BJN19930105","article-title":"Nutrition and growth of suckling black bears (Ursus americanus) during their mothers\u2019 winter fast","volume":"70","author":"Oftedal","year":"1993","journal-title":"Br. J. Nutr."},{"key":"2021042508445765100_JEB120725C31","first-page":"3","article-title":"Practical approach to bone biopsy","volume-title":"Bone Histomorphometry: Techniques and Interpretation","author":"Rao","year":"1983"},{"key":"2021042508445765100_JEB120725C32","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1007\/BF02556365","article-title":"Ultrasonic measurement of immobilization-induced osteopenia: an experimental study in sheep","volume":"42","author":"Rubin","year":"1988"},{"key":"2021042508445765100_JEB120725C33","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.1016\/j.bone.2011.08.017","article-title":"Investigating the mechanism for maintaining eucalcemia despite immobility and anuria in the hibernating American black bear (Ursus americanus)","volume":"49","author":"Seger","year":"2011","journal-title":"Bone"},{"key":"2021042508445765100_JEB120725C34","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1016\/j.bone.2011.10.001","article-title":"Central and peripheral mechanisms of the NPY system in the regulation of bone and adipose tissue","volume":"50","author":"Shi","year":"2012","journal-title":"Bone"},{"key":"2021042508445765100_JEB120725C35","doi-asserted-by":"publisher","first-page":"3933","DOI":"10.1210\/en.2008-0109","article-title":"Cocaine and amphetamine-regulated transcript may regulate bone remodeling as a circulating molecule","volume":"149","author":"Singh","year":"2008","journal-title":"Endocrinology"},{"key":"2021042508445765100_JEB120725C36","doi-asserted-by":"publisher","first-page":"906","DOI":"10.1126\/science.1199435","article-title":"Hibernation in black bears: independence of metabolic suppression from body temperature","volume":"331","author":"Toien","year":"2011","journal-title":"Science"},{"key":"2021042508445765100_JEB120725C37","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1152\/japplphysiol.01622.2005","article-title":"Disuse in adult male rats attenuates the bone anabolic response to a therapeutic dose of parathyroid hormone","volume":"101","author":"Turner","year":"2006","journal-title":"J. Appl. Physiol."},{"key":"2021042508445765100_JEB120725C38","doi-asserted-by":"publisher","first-page":"2141","DOI":"10.1046\/j.1523-1755.1999.00461.x","article-title":"Circulating biochemical markers of bone remodeling in uremic patients","volume":"55","author":"Urena","year":"1999","journal-title":"Kidney Int."},{"key":"2021042508445765100_JEB120725C39","doi-asserted-by":"publisher","first-page":"1771","DOI":"10.1359\/JBMR.040811","article-title":"Intravenous pamidronate prevents femoral bone loss and renal stone formation during 90-day bed rest","volume":"19","author":"Watanabe","year":"2004","journal-title":"J. Bone Miner. Res."},{"key":"2021042508445765100_JEB120725C40","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/8756-3282(89)90052-5","article-title":"Osteopenia in the immobilized rat hind limb is associated with increased bone resorption and decreased bone formation","volume":"10","author":"Weinreb","year":"1989","journal-title":"Bone"}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/218\/13\/2067\/1911249\/jeb120725.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/218\/13\/2067\/1911249\/jeb120725.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,25]],"date-time":"2021-04-25T06:01:29Z","timestamp":1619330489000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/218\/13\/2067\/13816\/Suppressed-bone-remodeling-in-black-bears"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,7,1]]},"references-count":41,"journal-issue":{"issue":"13","published-print":{"date-parts":[[2015,7,1]]}},"URL":"https:\/\/doi.org\/10.1242\/jeb.120725","relation":{},"ISSN":["1477-9145","0022-0949"],"issn-type":[{"value":"1477-9145","type":"electronic"},{"value":"0022-0949","type":"print"}],"subject":[],"published":{"date-parts":[[2015,7,1]]}}}