{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T14:08:15Z","timestamp":1770818895619,"version":"3.50.1"},"reference-count":34,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[1998,2,1]],"date-time":"1998-02-01T00:00:00Z","timestamp":886291200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[1998,2,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>We examined associations of biochemical markers of bone turnover with rapid bone loss, as measured by changes in bone mineral density (BMD). To improve the precision of bone loss estimates, calcaneal BMD was measured up to eight times over a long interval (13 years) among postmenopausal women (mean age = 62 years at baseline). Women with fractures during the previous year, and users of corticosteroids, active vitamin D, bisphosphonates or calcitonin were excluded to avoid potential transient effects on marker levels. Among the remaining 354 women, markers were measured for 100 women with the fastest BMD loss (rapid loss group; mean = 2.2%\/year) and 100 with the slowest loss (mean = 0.4%\/year). Two markers of bone formation, serum bone alkaline phosphatase (Alkphase-B; BAP) and osteocalcin (NovoCalcin; OC), and two markers of bone resorption, urinary creatinine-corrected free deoxypyridinoline (Pyrilinks-D; DPD) and free pyridinolines (Pyrilinks; PYD), were measured. In separate logistic regression models, each of the markers was strongly associated with rapid loss: the odds of rapid loss increased by 1.8 to 2.0 times for each 1.0 standard deviation (SD) increase of the marker. For BAP levels 2 SD above the mean, the probability of rapid bone loss was 80%; in contrast, the probability was only 20% at 2 SD below the mean. The other markers yielded similar results. We conclude that these markers are associated with rapid bone loss; this relationship appears to be continuous, with progressively greater risk of rapid bone loss with increasing levels of biomarkers. Prospective studies that include the entire distribution of bone loss rates are warranted to confirm these findings.<\/jats:p>","DOI":"10.1359\/jbmr.1998.13.2.297","type":"journal-article","created":{"date-parts":[[2006,4,27]],"date-time":"2006-04-27T00:17:25Z","timestamp":1146097045000},"page":"297-302","source":"Crossref","is-referenced-by-count":188,"title":["Rapid Bone Loss Is Associated with Increased Levels of Biochemical Markers"],"prefix":"10.1093","volume":"13","author":[{"given":"Philip D.","family":"Dr. Ross","sequence":"first","affiliation":[{"name":"Hawaii Osteoporosis Foundation, Honolulu, Hawaii, U.S.A."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"William","family":"Knowlton","sequence":"additional","affiliation":[{"name":"Hawaii Osteoporosis Foundation, Honolulu, Hawaii, U.S.A."}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2009,12,4]]},"reference":[{"key":"2024020713324777200_bib1","doi-asserted-by":"crossref","first-page":"1531","DOI":"10.1002\/jbmr.5650111021","article-title":"Markers of bone resorption predict hip fracture in elderly women: The EPIDOS prospective study","volume":"11","author":"Garnero","year":"1996","journal-title":"J Bone Miner Res"},{"issue":"Suppl 1","key":"2024020713324777200_bib2","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/BF02500136","article-title":"Undercarboxylated osteocalcin (ucOC) measured with a direct and specific immunoassay predicts hip fracture (fx) in elderly women: The EPIDOS prospective study","volume":"6","author":"Vergnaud","year":"1996","journal-title":"Osteoporos Int"},{"key":"2024020713324777200_bib3","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1136\/bmj.312.7029.482","article-title":"Case-control analysis of bone resorption markers, disability, and hip fracture risk: The Rotterdam study","volume":"312","author":"van Daele","year":"1996","journal-title":"Br Med J"},{"issue":"Suppl 1","key":"2024020713324777200_bib4","first-page":"128","article-title":"Urine markers of bone resorption predict hip bone loss and fractures in older women: The Study of Osteoporotic Fractures","volume":"11","author":"Cummings","year":"1996","journal-title":"J Bone Miner Res"},{"key":"2024020713324777200_bib5","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/8756-3282(96)00037-3","article-title":"Serum undercarboxylated osteocalcin is a marker of the risk of hip fracture: A three year follow-up study","volume":"18","author":"Szulc","year":"1996","journal-title":"Bone"},{"issue":"Suppl. 1","key":"2024020713324777200_bib6","doi-asserted-by":"crossref","first-page":"S199","DOI":"10.1007\/BF02500333","article-title":"Evidence for uncoupling of bone formation and bone resorption in women with hip fractures: A prospective study","volume":"6","author":"van Daele","year":"1996","journal-title":"Osteoporos Int"},{"key":"2024020713324777200_bib7","author":"Sklarin","year":"1996"},{"key":"2024020713324777200_bib8","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1136\/bmj.303.6808.961","article-title":"Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 years study","volume":"303","author":"Hansen","year":"1991","journal-title":"Br Med J"},{"key":"2024020713324777200_bib9","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/8756-3282(96)00102-0","article-title":"Low bone mass and fast rate of bone loss at menopause: Equal risk factors for future fracture: A 15-year follow-up study","volume":"19","author":"Riis","year":"1996","journal-title":"Bone"},{"key":"2024020713324777200_bib10","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1002\/jbmr.5650101127","article-title":"Assessment of biochemical markers of bone metabolism in relation to the occurrence of fracture: A retrospective and prospective population-based study of women","volume":"10","author":"Akesson","year":"1995","journal-title":"J Bone Miner Res"},{"key":"2024020713324777200_bib11","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1172\/JCI113725","article-title":"Bone turnover in postmenopausal osteoporosis: Effect of calcitonin treatment","volume":"82","author":"Civitelli","year":"1988","journal-title":"J Clin Invest"},{"key":"2024020713324777200_bib12","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1359\/jbmr.1997.12.4.624","article-title":"The usefulness of bone turnover in predicting the response to transdermal estrogen therapy in postmenopausal osteoporosis","volume":"12","author":"Gonnelli","year":"1997","journal-title":"J Bone Miner Res"},{"key":"2024020713324777200_bib13","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0002-9343(96)00387-7","article-title":"Hormone replacement therapy in postmenopausal women: Urinary N-telopeptide of type I collagen monitors therapeutic effect and predicts response to bone mineral density","volume":"102","author":"Chesnut","year":"1997","journal-title":"Am J Med"},{"key":"2024020713324777200_bib14","first-page":"33S","article-title":"The usefulness of bone turnover in predicting the response to alendronate in postmenopausal osteoporosis","volume":"20","author":"Gonnelli","year":"1997","journal-title":"Bone"},{"key":"2024020713324777200_bib15","doi-asserted-by":"crossref","first-page":"197S","DOI":"10.1016\/8756-3282(95)00502-1","article-title":"Drug therapy for vertebral fractures in osteoporosis: Evidence that decreases in bone turnover and increases in bone mass both determine antifracture efficacy","volume":"18","author":"Riggs","year":"1996","journal-title":"Bone"},{"key":"2024020713324777200_bib16","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1093\/oxfordjournals.aje.a113796","article-title":"Bone mineral measurements among middle-aged and elderly Japanese residents in Hawaii","volume":"119","author":"Yano","year":"1984","journal-title":"Am J Epidemiol"},{"key":"2024020713324777200_bib17","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/0895-4356(91)90034-7","article-title":"Characteristics of respondents and nonrespondents in a prospective study of osteoporosis","volume":"44","author":"Heilbrun","year":"1991","journal-title":"J Clin Epidemiol"},{"key":"2024020713324777200_bib18","first-page":"476","article-title":"Marked diurnal variation in urinary excretion of pyridinium cross-links in premenopausal women","volume":"74","author":"Schlemmer","year":"1992","journal-title":"J Clin Endocrinol Metab"},{"key":"2024020713324777200_bib19","first-page":"487","article-title":"Abnormalities in circadian patterns of bone resorption and renal calcium conservation in type I osteoporosis","volume":"74","author":"Eastell","year":"1992","journal-title":"J Clin Endocrinol Metab"},{"key":"2024020713324777200_bib20","doi-asserted-by":"crossref","first-page":"1570","DOI":"10.1093\/clinchem\/43.9.1570","article-title":"Comparison of analytical performance and biological variability of three bone resorption assays","volume":"43","author":"Ju","year":"1997","journal-title":"Clin Chem"},{"key":"2024020713324777200_bib21","first-page":"319","volume-title":"Osteoporosis: Etiology, Diagnosis, and Management","author":"Delmas","year":"1995","edition":"2nd Ed."},{"key":"2024020713324777200_bib22","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1002\/jbmr.5650110307","article-title":"Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis","volume":"11","author":"Garnero","year":"1996","journal-title":"J Bone Miner Res"},{"key":"2024020713324777200_bib23","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/8756-3282(96)00201-3","article-title":"High bone turnover is associated with low bone mass in both pre- and postmenopausal women","volume":"19","author":"Ravn","year":"1996","journal-title":"Bone"},{"key":"2024020713324777200_bib24","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1007\/s002239900225","article-title":"High bone turnover is associated with low bone mass and spinal fracture in postmenopausal women","volume":"60","author":"Ravn","year":"1997","journal-title":"Calcif Tissue Int"},{"key":"2024020713324777200_bib25","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1111\/j.1365-2362.1988.tb02412.x","article-title":"Plasma BGP: An indicator of spontaneous bone loss and effect of estrogen treatment in postmenopausal women","volume":"18","author":"Johansen","year":"1988","journal-title":"Eur J Clin Invest"},{"key":"2024020713324777200_bib26","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1007\/BF02508642","article-title":"Bone density change and biochemical indices of skeletal turnover","volume":"58","author":"Cosman","year":"1996","journal-title":"Calcif Tissue Int"},{"key":"2024020713324777200_bib27","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1007\/s002239900135","article-title":"Biochemical markers of bone turnover reflect femoral bone loss in elderly women","volume":"59","author":"Dresner-Pollak","year":"1996","journal-title":"Calcif Tissue Int"},{"key":"2024020713324777200_bib28","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1210\/jcem-72-2-367","article-title":"Effect of menopause and hormone replacement therapy on the urinary excretion of pyridinium crosslinks","volume":"72","author":"Uebelhart","year":"1991","journal-title":"J Clin Endocrinol Metab"},{"key":"2024020713324777200_bib29","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1172\/JCI118382","article-title":"Sex steroids, bone mass, and bone loss: A prospective study of pre- peri- and postmenopausal women","volume":"97","author":"Slemenda","year":"1996","journal-title":"J Clin Invest"},{"key":"2024020713324777200_bib30","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1007\/BF01623014","article-title":"Can biochemical markers predict bone loss at the hip and spine? A 4-year prospective study of 141 early postmenopausal women","volume":"6","author":"Keen","year":"1996","journal-title":"Osteoporos Int"},{"key":"2024020713324777200_bib31","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1007\/BF03349795","article-title":"Temporal relationship between bone loss and increased bone turnover: A longitudinal study following natural menopause","volume":"18","author":"Rosso","year":"1995","journal-title":"J Endocrinol Invest"},{"key":"2024020713324777200_bib32","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1111\/j.1365-2265.1994.tb02512.x","article-title":"Urinary excretion of pyridinium cross-links in healthy women: The long-term effects of menopause and oestrogen\/progesterone therapy","volume":"40","author":"Schlemmer","year":"1994","journal-title":"Clin Endocrinol"},{"key":"2024020713324777200_bib33","doi-asserted-by":"crossref","first-page":"919","DOI":"10.7326\/0003-4819-114-11-919","article-title":"Pre-existing fractures and bone mass predict vertebral fracture incidence","volume":"114","author":"Ross","year":"1991","journal-title":"Ann Intern Med"},{"key":"2024020713324777200_bib34","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1136\/bmj.312.7041.1254","article-title":"Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures","volume":"312","author":"Marshall","year":"1996","journal-title":"Br Med J"}],"container-title":["Journal of Bone and Mineral Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1359%2Fjbmr.1998.13.2.297","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/13\/2\/297\/56599415\/5650130217.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/13\/2\/297\/56599415\/5650130217.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,13]],"date-time":"2024-03-13T14:56:14Z","timestamp":1710341774000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jbmr\/article\/13\/2\/297-302\/7514543"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1998,2,1]]},"references-count":34,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2009,12,4]]},"published-print":{"date-parts":[[1998,2,1]]}},"URL":"https:\/\/doi.org\/10.1359\/jbmr.1998.13.2.297","relation":{},"ISSN":["0884-0431","1523-4681"],"issn-type":[{"value":"0884-0431","type":"print"},{"value":"1523-4681","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[1998,2,1]]},"published":{"date-parts":[[1998,2,1]]}}}