{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T22:01:59Z","timestamp":1792792919511,"version":"4.5.0"},"reference-count":38,"publisher":"The Endocrine Society","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2017,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Context<\/jats:title>\n                    <jats:p>Sleep abnormalities are associated with low bone mineral density. Underlying mechanisms are unknown.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>Investigate the impact of sleep restriction with circadian disruption on bone biomarkers.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Design<\/jats:title>\n                    <jats:p>Intervention study.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Participants and Methods<\/jats:title>\n                    <jats:p>Four bone biomarkers [C-terminal cross-linked telopeptide of type I collagen (CTX) = bone resorption, N-terminal propeptide of type I procollagen (P1NP) = bone formation, sclerostin and fibroblast growth factor 23 = osteocyte function] were measured in bihourly serum samples over 24 hours at baseline and after \u223c3 weeks of sleep restriction (5.6 hours sleep\/24 hours) with concurrent circadian disruption (recurring 28-hour \u201cday\u201d in dim light) in 10 men (age groups: 20 to 27 years, n = 6; 55 to 65 years, n = 4). The effects of sleep\/circadian disruption and age on bone biomarker levels were evaluated using maximum likelihood estimation in a mixed model for repeated measures.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>P1NP levels were lower after intervention compared with baseline (P &amp;lt; 0.001); the decrease in P1NP was greater for younger compared with older men (28.0% vs 18.2%, P &amp;lt; 0.001). There was no change in CTX (\u0394 = 0.03 \u00b1 0.02 ng\/mL, P = 0.10). Sclerostin levels were higher postintervention in the younger men only (\u0394 = 22.9% or 5.64 \u00b1 1.10 pmol\/L, P &amp;lt; 0.001).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>These data suggest that 3 weeks of circadian disruption with concurrent sleep restriction can lead to an uncoupling of bone turnover wherein bone formation is decreased but bone resorption is unchanged. Circadian disruption and sleep restriction may be most detrimental to bone in early adulthood.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1210\/jc.2017-01147","type":"journal-article","created":{"date-parts":[[2017,7,26]],"date-time":"2017-07-26T14:04:34Z","timestamp":1501077874000},"page":"3722-3730","source":"Crossref","is-referenced-by-count":94,"title":["Bone Turnover Markers After Sleep Restriction and Circadian Disruption: A Mechanism for Sleep-Related Bone Loss in Humans"],"prefix":"10.1210","volume":"102","author":[{"given":"Christine M","family":"Swanson","sequence":"first","affiliation":[{"name":"Division of Endocrinology and Bone and Mineral Unit, Oregon Health & Science University, Portland, Oregon 97239"},{"name":"Division of Endocrinology, University of Colorado, Aurora, Colorado 80045"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven A","family":"Shea","sequence":"additional","affiliation":[{"name":"Oregon Institute of Occupational Health Sciences, Oregon Health & Science University, Portland, Oregon 97239"},{"name":"Sleep Health Institute, Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women\u2019s Hospital, Boston, Massachusetts 02115"},{"name":"Oregon Health & Science University and Portland State University School of Public Health, Portland, Oregon 97239"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pamela","family":"Wolfe","sequence":"additional","affiliation":[{"name":"Department of Biostatistics and Informatics, Colorado School of Public Health, University of Colorado Anschutz Medical Campus, Aurora, Colorado 80045"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sean W","family":"Cain","sequence":"additional","affiliation":[{"name":"Sleep Health Institute, Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women\u2019s Hospital, Boston, Massachusetts 02115"},{"name":"Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts 02115"},{"name":"Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirjam","family":"Munch","sequence":"additional","affiliation":[{"name":"Charit\u00e9 University Medicine Berlin, Institute of Physiology, 10117 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nina","family":"Vujovi\u0107","sequence":"additional","affiliation":[{"name":"Sleep Health Institute, Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women\u2019s Hospital, Boston, Massachusetts 02115"},{"name":"Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts 02115"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles A","family":"Czeisler","sequence":"additional","affiliation":[{"name":"Sleep Health Institute, Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women\u2019s Hospital, Boston, Massachusetts 02115"},{"name":"Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts 02115"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Orfeu M","family":"Buxton","sequence":"additional","affiliation":[{"name":"Sleep Health Institute, Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women\u2019s Hospital, Boston, Massachusetts 02115"},{"name":"Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts 02115"},{"name":"Department of Biobehavioral Health, Pennsylvania State University, University Park, Pennsylvania 16802"},{"name":"Department of Social and Behavioral Sciences, Harvard Chan School of Public Health, Boston, Massachusetts 02115"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric S","family":"Orwoll","sequence":"additional","affiliation":[{"name":"Division of Endocrinology and Bone and Mineral Unit, Oregon Health & Science University, Portland, Oregon 97239"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"80","published-online":{"date-parts":[[2017,7,26]]},"reference":[{"issue":"2","key":"2020071622420029100_B1","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1002\/jbmr.2446","article-title":"Obstructive sleep apnea and metabolic bone disease: insights into the relationship between bone and sleep","volume":"30","author":"Swanson","year":"2015","journal-title":"J Bone Miner Res"},{"issue":"5","key":"2020071622420029100_B2","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1016\/j.bone.2011.08.008","article-title":"Association between sleep duration and bone mineral density in Chinese women","volume":"49","author":"Fu","year":"2011","journal-title":"Bone"},{"issue":"7","key":"2020071622420029100_B3","doi-asserted-by":"crossref","first-page":"1401","DOI":"10.1111\/jgs.13477","article-title":"Is self-reported sleep duration associated with osteoporosis? Data from a 4-year aggregated analysis from the National Health and Nutrition Examination Survey","volume":"63","author":"Cunningham","year":"2015","journal-title":"J Am Geriatr Soc"},{"issue":"2","key":"2020071622420029100_B4","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1007\/s11325-011-0545-6","article-title":"Association between osteoporosis and sleep duration in healthy middle-aged and elderly adults: a large-scale, cross-sectional study in Japan","volume":"16","author":"Kobayashi","year":"2011","journal-title":"Sleep Breath"},{"issue":"7","key":"2020071622420029100_B5","doi-asserted-by":"crossref","first-page":"e0132342","DOI":"10.1371\/journal.pone.0132342","article-title":"Association between sleep duration, insomnia symptoms and bone mineral density in older Boston Puerto Rican adults","volume":"10","author":"Niu","year":"2015","journal-title":"PLoS One"},{"issue":"11","key":"2020071622420029100_B6","doi-asserted-by":"crossref","first-page":"2641","DOI":"10.1007\/s00198-015-3172-4","article-title":"Sleep duration and timing in relation to osteoporosis in an elderly Chinese population: a cross-sectional analysis in the Dongfeng-Tongji cohort study","volume":"26","author":"Tian","year":"2015","journal-title":"Osteoporos Int"},{"issue":"11","key":"2020071622420029100_B7","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.5664\/jcsm.6266","article-title":"Does subjective sleep affect bone mineral density in older people with minimal health disorders? The PROOF Cohort","volume":"12","author":"Saint Martin","year":"2016","journal-title":"J Clin Sleep Med"},{"issue":"8","key":"2020071622420029100_B8","doi-asserted-by":"crossref","first-page":"2869","DOI":"10.1210\/jc.2013-3629","article-title":"Associations between sleep duration, daytime nap duration, and osteoporosis vary by sex, menopause, and sleep quality","volume":"99","author":"Chen","year":"2014","journal-title":"J Clin Endocrinol Metab"},{"issue":"2","key":"2020071622420029100_B9","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1007\/s12020-014-0493-6","article-title":"The associations of bedtime, nocturnal, and daytime sleep duration with bone mineral density in pre- and post-menopausal women","volume":"49","author":"Wang","year":"2014","journal-title":"Endocrine"},{"issue":"12","key":"2020071622420029100_B10","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1001\/jama.2013.277817","article-title":"Repeat bone mineral density screening and prediction of hip and major osteoporotic fracture","volume":"310","author":"Berry","year":"2013","journal-title":"JAMA"},{"issue":"10","key":"2020071622420029100_B11","doi-asserted-by":"crossref","first-page":"1853","DOI":"10.1111\/jgs.13069","article-title":"Hypoxia during sleep and the risk of falls and fractures in older men: the Osteoporotic Fractures in Men Sleep Study","volume":"62","author":"Cauley","year":"2014","journal-title":"J Am Geriatr Soc"},{"issue":"4","key":"2020071622420029100_B12","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1007\/s00198-008-0729-5","article-title":"Nightshift work and fracture risk: the Nurses\u2019 Health Study","volume":"20","author":"Feskanich","year":"2008","journal-title":"Osteoporos Int"},{"issue":"1","key":"2020071622420029100_B13","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/S8756-3282(02)00791-3","article-title":"Circadian variation in the serum concentration of C-terminal telopeptide of type I collagen (serum CTx): effects of gender, age, menopausal status, posture, daylight, serum cortisol, and fasting","volume":"31","author":"Qvist","year":"2002","journal-title":"Bone"},{"issue":"129","key":"2020071622420029100_B14","doi-asserted-by":"crossref","first-page":"129ra43","DOI":"10.1126\/scitranslmed.3003200","article-title":"Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption","volume":"4","author":"Buxton","year":"2012","journal-title":"Sci Transl Med"},{"issue":"1","key":"2020071622420029100_B15","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/0304-3940(94)90841-9","article-title":"Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans","volume":"166","author":"Dijk","year":"1994","journal-title":"Neurosci Lett"},{"key":"2020071622420029100_B16","article-title":"24-Hour profile of serum sclerostin and its association with bone biomarkers in men [published online ahead of print May 26, 2017]","volume-title":"Osteoporos Int","author":"Swanson"},{"key":"2020071622420029100_B17","unstructured":"Kainos Laboratories. FGF-23 ELISA kit insert. Available at: http:\/\/www.kainos.co.jp\/eng\/products\/fgf23_e\/fgf23_e_4.html. Accessed 28 January 2014."},{"issue":"1","key":"2020071622420029100_B18","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1373\/clinchem.2007.094953","article-title":"Evaluation of a fully automated serum assay for total N-terminal propeptide of type I collagen in postmenopausal osteoporosis","volume":"54","author":"Garnero","year":"2007","journal-title":"Clin Chem"},{"issue":"8","key":"2020071622420029100_B19","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1093\/clinchem\/47.8.1410","article-title":"Clinical evaluation of the Elecsys beta-CrossLaps serum assay, a new assay for degradation products of type I collagen C-tlopeptides","volume":"47","author":"Okabe","year":"2001","journal-title":"Clin Chem"},{"key":"2020071622420029100_B20","volume-title":"Designing Clinical Research","author":"Hulley","edition":"4th ed."},{"issue":"9","key":"2020071622420029100_B21","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1258\/ebm.2012.012043","article-title":"Chronically inadequate sleep results in abnormal bone formation and abnormal bone marrow in rats","volume":"237","author":"Everson","year":"2012","journal-title":"Exp Biol Med (Maywood)"},{"issue":"1","key":"2020071622420029100_B22","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/s13018-016-0418-6","article-title":"Effects of chronic sleep deprivation on bone mass and bone metabolism in rats","volume":"11","author":"Xu","year":"2016","journal-title":"J Orthop Surg"},{"issue":"9","key":"2020071622420029100_B23","doi-asserted-by":"crossref","first-page":"2159","DOI":"10.1007\/s00198-014-2646-0","article-title":"PINP as a biological response marker during teriparatide treatment for osteoporosis","volume":"25","author":"Krege","year":"2014","journal-title":"Osteoporos Int"},{"issue":"1","key":"2020071622420029100_B24","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1185\/030079905X75096","article-title":"Development of an algorithm for using PINP to monitor treatment of patients with teriparatide","volume":"22","author":"Eastell","year":"2005","journal-title":"Curr Med Res Opin"},{"issue":"4","key":"2020071622420029100_B25","doi-asserted-by":"crossref","first-page":"798","DOI":"10.1016\/j.bone.2010.12.006","article-title":"PINP as an aid for monitoring patients treated with teriparatide","volume":"48","author":"Tsujimoto","year":"2011","journal-title":"Bone"},{"issue":"12","key":"2020071622420029100_B26","doi-asserted-by":"crossref","first-page":"2971","DOI":"10.1007\/s00198-013-2379-5","article-title":"Early changes in biochemical markers of bone formation during teriparatide therapy correlate with improvements in vertebral strength in men with glucocorticoid-induced osteoporosis","volume":"24","author":"Farahmand","year":"2013","journal-title":"Osteoporos Int"},{"key":"2020071622420029100_B27","doi-asserted-by":"crossref","first-page":"1573","DOI":"10.1016\/B978-0-12-415853-5.00067-4","volume-title":"Osteoporosis","author":"Szulc","year":"2013","edition":"4th ed."},{"issue":"11","key":"2020071622420029100_B28","doi-asserted-by":"crossref","first-page":"2251","DOI":"10.1007\/s00421-014-2950-6","article-title":"Bone formation is suppressed with multi-stressor military training","volume":"114","author":"Hughes","year":"2014","journal-title":"Eur J Appl Physiol"},{"issue":"11","key":"2020071622420029100_B29","doi-asserted-by":"crossref","first-page":"S623","DOI":"10.1249\/MSS.0b013e3181892dc2","article-title":"How stress fracture incidence was lowered in the Israeli army: a 25-yr struggle","volume":"40","author":"Finestone","year":"2008","journal-title":"Med Sci Sports Exerc"},{"issue":"1","key":"2020071622420029100_B30","first-page":"33","article-title":"Skeletal responses to space flight and the bed rest analog: a review","volume":"7","author":"LeBlanc","year":"2007","journal-title":"J Musculoskelet Neuronal Interact"},{"issue":"3","key":"2020071622420029100_B31","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1007\/s00774-015-0681-3","article-title":"Serum sclerostin and DKK1 in relation to exercise against bone loss in experimental bed rest","volume":"34","author":"Belav\u00fd","year":"2015","journal-title":"J Bone Miner Metab"},{"issue":"1","key":"2020071622420029100_B32","first-page":"399","article-title":"Markers of bone metabolism during 14 days of bed rest in young and older men","volume":"17","author":"Buehlmeier","year":"2017","journal-title":"J Musculoskelet Neuronal Interact"},{"issue":"4","key":"2020071622420029100_B33","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1016\/j.jacc.2003.07.050","article-title":"Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk","volume":"43","author":"Meier-Ewert","year":"2004","journal-title":"J Am Coll Cardiol"},{"issue":"7","key":"2020071622420029100_B34","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1359\/jbmr.070409","article-title":"Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study","volume":"22","author":"Cauley","year":"2007","journal-title":"J Bone Miner Res"},{"issue":"10","key":"2020071622420029100_B35","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1016\/j.cub.2012.03.038","article-title":"Social jetlag and obesity","volume":"22","author":"Roenneberg","year":"2012","journal-title":"Curr Biol"},{"issue":"12","key":"2020071622420029100_B36","doi-asserted-by":"crossref","first-page":"4662","DOI":"10.1210\/jc.2015-2957","article-title":"Are biochemical markers of bone turnover representative of bone histomorphometry in 370 postmenopausal women?","volume":"100","author":"Chavassieux","year":"2015","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071622420029100_B37","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bone.2013.10.019","article-title":"Effects of age on bone mRNA levels of sclerostin and other genes relevant to bone metabolism in humans","volume":"59","author":"Roforth","year":"2014","journal-title":"Bone"},{"key":"2020071622420029100_B38","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1038\/bonekey.2013.95","article-title":"Clinical utility of serum sclerostin measurements","volume":"2","author":"Clarke","year":"2013","journal-title":"Bonekey Rep"}],"container-title":["The Journal of Clinical Endocrinology &amp; Metabolism"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jcem\/article-pdf\/102\/10\/3722\/20619993\/jc.2017-01147.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jcem\/article-pdf\/102\/10\/3722\/20619993\/jc.2017-01147.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,7,17]],"date-time":"2020-07-17T07:10:39Z","timestamp":1594969839000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jcem\/article\/102\/10\/3722\/4036362"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,7,26]]},"references-count":38,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2017,10,1]]}},"URL":"https:\/\/doi.org\/10.1210\/jc.2017-01147","relation":{},"ISSN":["0021-972X","1945-7197"],"issn-type":[{"value":"0021-972X","type":"print"},{"value":"1945-7197","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2017,10,1]]},"published":{"date-parts":[[2017,7,26]]}}}