{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T22:46:53Z","timestamp":1791326813677,"version":"4.3.1"},"reference-count":55,"publisher":"Oxford University Press (OUP)","issue":"9","license":[{"start":{"date-parts":[[2001,9,1]],"date-time":"2001-09-01T00:00:00Z","timestamp":999302400000},"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":[[2001,9,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>We describe a sinus, referred to as a bone remodeling compartment (BRC), which is intimately associated with cancellous bone remodeling. The compartment is lined on its marrow side by flattened cells and on its osseous side by the remodeling bone surface, resembling a roof of flattened cells covering the bone surface. The flat marrow lining cells are in continuity with the bone lining cells at the margins of the BRC. We examined a large number of diagnostic bone biopsy specimens received during recent years in the department. Furthermore, 10 patients (8 women and 2 men, median age 56 [40\u201369] years) with the high turnover disease of primary hyperparathyroidism who were treated with parathyroidectomy and followed for 3 years were included in the histomorphometric study. Bone samples for the immuno-enzyme staining were obtained from an amputated extremity of child. The total cancellous bone surface covered by BRC decreases by 50% (p &amp;lt; 0.05) following normalization of turnover and is paralleled by a similar 50% decrease in remodeling surface (p &amp;lt; 0.05). The entire eroded surface and two-thirds of the osteoid surface are covered by a BRC. BRC-covered uncompleted walls are 30% (p &amp;lt; 0.05) thinner than those without a BRC. This indicates that the BRC is invariably associated with the early phases of bone remodeling, that is, bone resorption, whereas it closes during the late part of bone formation. Immuno-enzyme staining shows that the flat marrow lining cells are positive for alkaline phosphatase, osteocalcin, and osteonectin, suggesting that they are bone cells. The first step in cancellous bone remodeling is thought to be the lining cells digesting the unmineralized matrix membrane followed by their disappearance and the arrival of the bone multicellular unit (BMU). We suggest that the lining cell barrier persists during bone remodeling; that the old lining cells become the marrow lining cells, allowing bone resorption and bone formation to proceed under a common roof of lining cells; that, at the end of bone formation, new bone lining cells derived from the flattened osteoblasts replace the marrow lining cells thereby closing the BRC; and that the two layers of lining cells eventually becomes a single layer. The integrity of the osteocyte-lining cell system is reestablished by the new generation of lining cells. The BRC most likely serves multiple purposes, including efficient exchange of matrix constituents and minerals, routing, monitoring, or modulating bone cell recruitment, and possibly the anatomical basis for the coupling of bone remodeling.<\/jats:p>","DOI":"10.1359\/jbmr.2001.16.9.1575","type":"journal-article","created":{"date-parts":[[2006,4,26]],"date-time":"2006-04-26T20:52:32Z","timestamp":1146084752000},"page":"1575-1582","source":"Crossref","is-referenced-by-count":332,"title":["Cancellous Bone Remodeling Occurs in Specialized Compartments Lined by Cells Expressing Osteoblastic Markers"],"prefix":"10.1093","volume":"16","author":[{"given":"Ellen M.","family":"Hauge","sequence":"first","affiliation":[{"name":"Department of Pathology, Aarhus University Hospital, Aarhus C, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dorte","family":"Qvesel","sequence":"additional","affiliation":[{"name":"Department of Pathology, Aarhus University Hospital, Aarhus C, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erik Fink","family":"Eriksen","sequence":"additional","affiliation":[{"name":"Department of Pathology, Aarhus University Hospital, Aarhus C, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leif","family":"Mosekilde","sequence":"additional","affiliation":[{"name":"Department of Pathology, Aarhus University Hospital, Aarhus C, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Flemming","family":"Melsen","sequence":"additional","affiliation":[{"name":"Department of Pathology, Aarhus University Hospital, Aarhus C, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2009,12,2]]},"reference":[{"key":"2024020714122703000_bib1","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1097\/00003086-196801000-00025","article-title":"Submicroscopic structure and functional aspects of the osteocyte","volume":"56","author":"Baud","year":"1968","journal-title":"Clin Orthop"},{"key":"2024020714122703000_bib2","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1002\/aja.1001290408","article-title":"Morphological and physiological considerations in a new concept of calcium transport in bone","volume":"129","author":"Talmage","year":"1970","journal-title":"Am J Anat"},{"key":"2024020714122703000_bib3","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1038\/206489a0","article-title":"Suggested sequential mode of control of changes in cell behaviour in adult bone remodeling","volume":"206","author":"Hattner","year":"1965","journal-title":"Nature"},{"key":"2024020714122703000_bib4","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1242\/jcs.76.1.155","article-title":"Bone cells predispose bone surfaces to resorption by exposure of mineral to osteoclastic contact","volume":"76","author":"Chambers","year":"1985","journal-title":"J Cell Sci"},{"key":"2024020714122703000_bib5","first-page":"159","volume-title":"Calcified Tissue, Structural, Functional and Metabolic Aspects","author":"Jaworski","year":"1971"},{"key":"2024020714122703000_bib6","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1002\/jcb.240550303","article-title":"Osteonal and hemi-osteonal remodeling: The spatial and temporal framework for signal traffic in adult human bone","volume":"55","author":"Parfitt","year":"1994","journal-title":"J Cell Biochem"},{"key":"2024020714122703000_bib7","first-page":"25","article-title":"The structure of bone tissues and the cellular control of their deposition","volume":"101","author":"Marotti","year":"1996","journal-title":"Ital J Anat Embryol"},{"key":"2024020714122703000_bib8","first-page":"2","volume-title":"Bone Circulation","author":"Burkhardt","year":"1984"},{"key":"2024020714122703000_bib9","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/0026-2862(73)90014-9","article-title":"Relationship of bone blood flow to bone resorption and growth in situ","volume":"6","author":"McClugage","year":"1973","journal-title":"Microvscular Research"},{"key":"2024020714122703000_bib10","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1159\/000145171","article-title":"Changes in vascular network during the formation of Haversian systems","volume":"106","author":"Marotti","year":"1980","journal-title":"Acta Anat"},{"key":"2024020714122703000_bib11","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/S8756-3282(00)80937-0","article-title":"The mechanism of coupling: A role for the vasculature","volume":"26","author":"Parfitt","year":"2000","journal-title":"Bone"},{"key":"2024020714122703000_bib12","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1016\/S8756-3282(00)00260-X","article-title":"Primary hyperparathyroidism: Bone structure, balance, and remodeling before and 3 years after surgical treatment","volume":"26","author":"Steiniche","year":"2000","journal-title":"Bone"},{"key":"2024020714122703000_bib13","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/S8756-3282(99)00194-5","article-title":"Missing observations in bone histomorphometry on osteoporosis. Implications and suggestions for an approach","volume":"25","author":"Hauge","year":"1999","journal-title":"Bone"},{"key":"2024020714122703000_bib14","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1111\/j.1365-2818.1986.tb04282.x","article-title":"Estimation of surface area from vertical sections","volume":"142","author":"Baddeley","year":"1986","journal-title":"J Microsc"},{"key":"2024020714122703000_bib15","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1002\/jbmr.5650020617","article-title":"Bone histomorphometry: Standardization of nomenclature, symbols, and units","volume":"2","author":"Parfitt","year":"1987","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib16","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/0221-8747(82)90024-8","article-title":"Estimation of the three-dimensional wall thickness of completed remodeling sites in iliac trabecular bone","volume":"4","author":"Kragstrup","year":"1982","journal-title":"Metab Bone Dis Relat Res"},{"key":"2024020714122703000_bib17","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/8756-3282(92)90004-G","article-title":"Reconstruction of the formative site in trabecular bone by a new, quick, and easy method","volume":"13","author":"Steiniche","year":"1992","journal-title":"Bone"},{"key":"2024020714122703000_bib18","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1177\/002215549704500215","article-title":"Embedding of bone samples in methylmethacrylate: An improved method suitable for bone histomorphometry, histochemistry, and immunohistochemistry","volume":"45","author":"Erben","year":"1997","journal-title":"J Histochem Cytochem"},{"key":"2024020714122703000_bib19","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1002\/jbmr.5650080902","article-title":"Distribution of noncollagenous proteins in the matrix of adult human bone: Evidence of anatomic and functional heterogeneity","volume":"8","author":"Ingram","year":"1993","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib20","first-page":"1587","article-title":"Fibrous dysplasia of bone in the McCune-Albright syndrome: Abnormalities in bone formation","volume":"151","author":"Riminucci","year":"1997","journal-title":"Am J Pathol"},{"key":"2024020714122703000_bib21","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1007\/BF00186987","article-title":"A study of intercellular relationships between trabecular bone and marrow stromal cells in the murine femoral metaphysis","volume":"192","author":"Yamazaki","year":"1995","journal-title":"Anat Embryol (Berl)"},{"key":"2024020714122703000_bib22","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/S0022-5320(74)80054-7","article-title":"The ultrastructure of the endosteum: A topographic study in young adult rabbits","volume":"46","author":"Luk","year":"1974","journal-title":"J Ultrastruct Res"},{"key":"2024020714122703000_bib23","first-page":"350","article-title":"The presence of lining cells on surfaces of human trabecular bone","volume":"134","author":"Vander Wiel","year":"1978","journal-title":"Clin Orthop"},{"key":"2024020714122703000_bib24","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1002\/ar.1091980204","article-title":"Characterization of endosteal bone-lining cells from fatty marrow bone sites in adult beagles","volume":"198","author":"Miller","year":"1980","journal-title":"Anat Rec"},{"key":"2024020714122703000_bib25","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1002\/ar.1092130211","article-title":"Bone lining cells and hematopoiesis: An electron microscopic study of canine bone marrow","volume":"213","author":"Deldar","year":"1985","journal-title":"Anat Rec"},{"key":"2024020714122703000_bib26","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1002\/1097-0185(20001201)260:4<410::AID-AR110>3.0.CO;2-Z","article-title":"Comparative morphology of the marrow sac","volume":"260","author":"Bi","year":"2000","journal-title":"Anat Rec"},{"key":"2024020714122703000_bib27","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1002\/ar.1092030114","article-title":"A cellular investment of bone marrow","volume":"203","author":"Menton","year":"1982","journal-title":"Anat Rec"},{"key":"2024020714122703000_bib28","volume-title":"The Physiological and Cellular Basis of Metabolic Bone Disease","author":"Rasmussen","year":"1974"},{"key":"2024020714122703000_bib29","doi-asserted-by":"crossref","first-page":"3632","DOI":"10.1210\/endo.136.8.7628403","article-title":"Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells","volume":"136","author":"Dobnig","year":"1995","journal-title":"Endocrinology"},{"key":"2024020714122703000_bib30","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1359\/jbmr.1998.13.11.1760","article-title":"Mechanical loading stimulates bone formation by reactivation of bone lining cells in 13-week-old rats","volume":"13","author":"Chow","year":"1998","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/jcp.1041400102","article-title":"Bone marrow-derived stromal cell line expressing osteoblastic phenotype in vitro and osteogenic capacity in vivo","volume":"140","author":"Benayahu","year":"1989","journal-title":"J Cell Physiol"},{"key":"2024020714122703000_bib32","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/BF02405298","article-title":"Distribution of fibroblastic colony-forming cells in rabbit bone marrow and assay of their osteogenic potential by an in vivo diffusion chamber method","volume":"36","author":"Ashton","year":"1984","journal-title":"Calcif Tissue Int"},{"key":"2024020714122703000_bib33","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1097\/00003086-197203000-00048","article-title":"Observations on two types of resorption cavities in human lamellar cortical bone","volume":"83","author":"Jaworski","year":"1972","journal-title":"Clin Orthop Rel Res"},{"key":"2024020714122703000_bib34","first-page":"143","volume-title":"Bone Histomorphometry: Techniques and Interpretation","author":"Parfitt","year":"1983","edition":"1st ed."},{"key":"2024020714122703000_bib35","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/8756-3282(93)90176-B","article-title":"Morphometry of bone resorption: Introduction and overview","volume":"14","author":"Parfitt","year":"1993","journal-title":"Bone"},{"key":"2024020714122703000_bib36","first-page":"S1; S237","article-title":"Cortical remodelling clusters (super-osteons) in the human femoral shaft","volume":"15","author":"Bell","year":"2000","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib37","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1016\/8756-3282(93)90179-E","article-title":"Histomorphometry of Howship's lacunae formed in vivo and in vitro: Depths and volumes measured by scanning electron and confocal microscopy","volume":"14","author":"Jones","year":"1993","journal-title":"Bone"},{"key":"2024020714122703000_bib38","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/0221-8747(83)90013-9","article-title":"Three-dimensional morphology of trabecular bone osteons reconstructed from serial sections","volume":"5","author":"Kragstrup","year":"1983","journal-title":"Metab Bone Dis Relat Res"},{"key":"2024020714122703000_bib39","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/S0169-6009(08)80165-1","article-title":"Stereological considerations concerning the measurements of individual osteoid seams and resorption cavities","volume":"26","author":"Hauge","year":"1994","journal-title":"Bone Miner"},{"key":"2024020714122703000_bib40","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1002\/jbmr.5650050106","article-title":"A control model for tibial cortex neovascularization in the bone chamber","volume":"5","author":"Winet","year":"1990","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib41","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1002\/ar.1092290404","article-title":"Rearrangement of the metaphyseal vasculature of the rat growth plate in rickets and rachitic reversal: A model of vascular arrest and angiogenesis renewed","volume":"229","author":"Hunter","year":"1991","journal-title":"Anat Rec"},{"key":"2024020714122703000_bib42","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1016\/8756-3282(86)90005-0","article-title":"Morphology of bone development and bone remodeling in embryonic chick limbs","volume":"7","author":"Pechak","year":"1986","journal-title":"Bone"},{"key":"2024020714122703000_bib43","doi-asserted-by":"crossref","first-page":"2936","DOI":"10.1073\/pnas.88.7.2936","article-title":"Osteoclastic inhibition\u2014an action of nitric oxide not mediated by cyclic GMP","volume":"88","author":"Macintyre","year":"1991","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024020714122703000_bib44","doi-asserted-by":"crossref","first-page":"3617","DOI":"10.1210\/endo.130.6.1597159","article-title":"Endothelin inhibits osteoclastic bone resorption by a direct effect on cell motility: Implications for the vascular control of bone resorption","volume":"130","author":"Alam","year":"1992","journal-title":"Endocrinology"},{"key":"2024020714122703000_bib45","doi-asserted-by":"crossref","first-page":"552","DOI":"10.3109\/17453676908989520","article-title":"Experimental limb disuse and bone blood flow","volume":"40","author":"Semb","year":"1969","journal-title":"Acta Orthop Scand"},{"key":"2024020714122703000_bib46","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/0221-8747(81)90042-4","article-title":"Skeletal blood flow in Paget's disease of bone","volume":"3","author":"Wootton","year":"1981","journal-title":"Metab Bone Dis Relat Res"},{"key":"2024020714122703000_bib47","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/8756-3282(87)90015-9","article-title":"Changes in trabecular bone, hematopoiesis and bone marrow vessels in aplastic anemia, primary osteoporosis, and old age: A comparative histomorphometric study","volume":"8","author":"Burkhardt","year":"1987","journal-title":"Bone"},{"key":"2024020714122703000_bib48","author":"M\u00f8ller","year":"1999"},{"key":"2024020714122703000_bib49","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1161\/01.ATV.17.7.1193","article-title":"Heterogeneity of endothelial cells. Specific markers","volume":"17","author":"Garlanda","year":"1997","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"2024020714122703000_bib50","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1016\/S0002-9440(10)65173-5","article-title":"Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry","volume":"155","author":"Maniotis","year":"1999","journal-title":"Am J Pathol"},{"key":"2024020714122703000_bib51","doi-asserted-by":"crossref","first-page":"1338","DOI":"10.1359\/jbmr.1999.14.8.1338","article-title":"Polarity of osteoblasts and osteoblast-like UMR-108 cells","volume":"14","author":"Ilvesaro","year":"1999","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib52","doi-asserted-by":"crossref","first-page":"832","DOI":"10.2106\/00004623-199173060-00006","article-title":"Early histological and ultrastructural changes in medullary fracture callus","volume":"73","author":"Brighton","year":"1991","journal-title":"J Bone Joint Surg (Am)"},{"key":"2024020714122703000_bib53","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1097\/00003086-199202000-00042","article-title":"Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis","volume":"275","author":"Diaz-Flores","year":"1992","journal-title":"Clin Orthop"},{"key":"2024020714122703000_bib54","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1359\/jbmr.1998.13.5.828","article-title":"Vascular pericytes express osteogenic potential in vitro and in vivo","volume":"13","author":"Doherty","year":"1998","journal-title":"J Bone Miner Res"},{"key":"2024020714122703000_bib55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S8756-3282(99)00241-0","article-title":"Toward a unifying theory of bone remodeling","volume":"26","author":"Martin","year":"2000","journal-title":"Bone"}],"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.2001.16.9.1575","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/16\/9\/1575\/56604018\/5650160901.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/16\/9\/1575\/56604018\/5650160901.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,13]],"date-time":"2024-03-13T15:03:26Z","timestamp":1710342206000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jbmr\/article\/16\/9\/1575-1582\/7515834"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2001,9,1]]},"references-count":55,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2009,12,2]]},"published-print":{"date-parts":[[2001,9,1]]}},"URL":"https:\/\/doi.org\/10.1359\/jbmr.2001.16.9.1575","relation":{},"ISSN":["0884-0431","1523-4681"],"issn-type":[{"value":"0884-0431","type":"print"},{"value":"1523-4681","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2001,9,1]]},"published":{"date-parts":[[2001,9,1]]}}}