Coupling of Bone Resorption and Formation in Real Time: New Knowledge Gained From Human Haversian BMUs
Open accessAbstract
It is well known that bone remodeling starts with a resorption event and ends with bone formation. However, what happens in between and how resorption and formation are coupled remains mostly unknown. Remodeling is achieved by so-called basic multicellular units (BMUs), which are local teams of osteoclasts, osteoblasts, and reversal cells recently proven identical with osteoprogenitors. Their organization within a BMU cannot be appropriately analyzed in common histology. The originality of the present study is to capture the events ranging from initiation of resorption to onset of formation as a functional continuum. It was based on the position of specific cell markers in longitudinal sections of Haversian BMUs generating new canals through human long bones. It showed that initial resorption at the tip of the canal is followed by a period where newly recruited reversal/osteoprogenitor cells and osteoclasts alternate, thus revealing the existence of a mixed “reversal-resorption” phase. Three-dimensional reconstructions obtained from serial sections indicated that initial resorption is mainly involved in elongating the canal and the additional resorption events in widening it. Canal diameter measurements show that the latter contribute the most to overall resorption. Of note, the density of osteoprogenitors continuously grew along the “reversal/resorption” surface, reaching at least 39 cells/mm on initiation of bone formation. This value was independent of the length of the reversal/resorption surface. These observations strongly suggest that bone formation is initiated only above a threshold cell density, that the length of the reversal/resorption period depends on how fast osteoprogenitor recruitment reaches this threshold, and thus that the slower the rate of osteoprogenitor recruitment, the more bone is degraded. They lead to a model where the newly recognized reversal/resorption phase plays a central role in the mechanism linking osteoprogenitor recruitment and the resorption-formation switch. © 2017 American Society for Bone and Mineral Research.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Secondary osteoclasts establish a functional link with reversal cells as focal bone remodeling progresses within a single BRC.
“first, primary osteoclasts have been identified at the cutting cone and secondary osteoclasts have been shown to establish a functional link with reversal cells (Figs. 1 and 3) as focal bone remodeling progresses within a single BRC,256”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [256]
Primary osteoclasts have been identified at the cutting cone.
“first, primary osteoclasts have been identified at the cutting cone and secondary osteoclasts have been shown to establish a functional link with reversal cells (Figs. 1 and 3) as focal bone remodeling progresses within a single BRC,256”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [256]
Lassen et al.'s findings indicate that a pure reversal period, as commonly depicted following a halt in resorption, does not take place.
“Lassen et al.’s256 findings indicate that a pure reversal period, as commonly depicted following a halt in resorption,8 does not take place.”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [256]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Dempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., Recker, R. R., & Parfitt, A. M. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1805 · Cited by 2,543 · see citing works
Romosozumab in Postmenopausal Women with Low Bone Mineral Density
McClung, M. R., Grauer, A., Boonen, S., Bolognese, M. A., Brown, J. P., Diez-Perez, A., Langdahl, B. L., Reginster, J.-Y., Zanchetta, J. R., Wasserman, S. M., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1305224 · Cited by 1,258 · see citing works
Parfitt, A. M. (1994) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240550303 · Cited by 1,001 · see citing works
Zebaze, R., Ghasemzadeh, A., Bohte, A., Iuliano-Burns, S., Mirams, M., Price, R. I., Mackie, E. J., & Seeman, E. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60320-0 · Cited by 870 · see citing works
Osteoclast–osteoblast communication
Matsuo, K., & Irie, N. (2008) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.03.027 · Cited by 780 · see citing works
ERIKSEN, E. F. (1986) · Endocrine Reviews · doi:10.1210/edrv-7-4-379 · Cited by 601 · see citing works
Osteocytes: master orchestrators of bone
Schaffler, M. B., Cheung, W.-Y., Majeska, R., & Kennedy, O. (2014) · Calcified Tissue International · doi:10.1007/s00223-013-9790-y · Cited by 514 · see citing works
The Bone Lining Cell: Its Role in Cleaning Howship's Lacunae and Initiating Bone Formation
Everts, V., Delaissé, J. M., Korper, W., Jansen, D. C., Tigchelaar-Gutter, W., Saftig, P., & Beertsen, W. (2002) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2002.17.1.77 · Cited by 411 · see citing works
Malaval, L., Modrowski, D., Gupta, A., & Aubin, J. E. (1994) · Journal of Cellular Physiology · doi:10.1002/jcp.1041580322 · Cited by 369 · see citing works
Jain, N., Iyer, K. V., Kumar, A., & Shivashankar, G. V. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300801110 · Cited by 362 · see citing works
A Physical Mechanism for Coupling Bone Resorption and Formation in Adult Human Bone
Andersen, T. L., Sondergaard, T. E., Skorzynska, K. E., Dagnaes-Hansen, F., Plesner, T. L., Hauge, E. M., Plesner, T., & Delaisse, J.-M. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.080627 · Cited by 325 · see citing works
Self-citationRecker, R. R., Benson, C., Matsumoto, T., Bolognese, M. A., Robins, D. A., Alam, J., Chiang, A. Y., Hu, L., Krege, J. H., Sowa, H., et al. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2351 · Cited by 295 · see citing works
Kim, S. W., Pajevic, P. D., Selig, M., Barry, K. J., Yang, J.-Y., Shin, C. S., Baek, W.-Y., Kim, J.-E., & Kronenberg, H. M. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1665 · Cited by 266 · see citing works
Parfitt, A. M., Villanueva, A. R., Foldes, J., & Rao, D. S. (1995) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650100319 · Cited by 231 · see citing works
Frost, H. M. (1964) · Medical Entomology and Zoology · Cited by 220 · see citing works
Age- and sex-related changes in iliac cortical bone mass and remodeling
Brockstedt, H. K., Kassem, M. S., Eriksen, E. F., Mosekilde, L., & Melsen, F. (1993) · Bone · doi:10.1016/8756-3282(93)90092-o · Cited by 210 · see citing works
Eriksen, E. F., Melsen, F., & Mosekilde, L. (1984) · Metabolic Bone Disease and Related Research · doi:10.1016/0221-8747(84)90065-1 · Cited by 196 · see citing works
McKee, M. D., Farach‐Carson, M. C., Butler, W. T., Hauschka, P. V., & Nanci, A. (1993) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650080413 · Cited by 193 · see citing works
The Three-Dimensional Anatomy of Haversian Systems
COHEN, J., & Harris, W. H. (1958) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-195840020-00015 · Cited by 190 · see citing works
Sims, N. A., & Martin, T. J. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00041 · Cited by 184 · see citing works
Lanyon, L. E., & Bourn, S. (1979) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-197961020-00019 · Cited by 176 · see citing works
Cortical Bone Porosity: What Is It, Why Is It Important, and How Can We Detect It?
Cooper, D. M. L., Kawalilak, C. E., Harrison, K. D., Johnston, B. D., & Johnston, J. D. (2016) · Current Osteoporosis Reports · doi:10.1007/s11914-016-0319-y · Cited by 173 · see citing works
Delaissé, J. (2014) · BoneKEy Reports · doi:10.1038/bonekey.2014.56 · Cited by 168 · see citing works
Effect of substrate composition on bone resorption by rabbit osteoclasts
Chambers, T. J., Thomson, B. M., & Fuller, K. (1984) · Journal of Cell Science · doi:10.1242/jcs.70.1.61 · Cited by 141 · see citing works
Understanding Coupling between Bone Resorption and Formation
Andersen, T. L., Abdelgawad, M. E., Kristensen, H. B., Hauge, E. M., Rolighed, L., Bollerslev, J., Kjærsgaard-Andersen, P., & Delaisse, J.-M. (2013) · The American Journal of Pathology · doi:10.1016/j.ajpath.2013.03.006 · Cited by 137 · see citing works
Self-citationA reconstruction of the remodelling cycle in normal human cortical iliac bone
Agerbæk, M., Eriksen, E. F., Kragstrup, J., Mosekilde, L., & Melsen, F. (1991) · Bone and Mineral · doi:10.1016/0169-6009(91)90039-3 · Cited by 105 · see citing works
The rate of osteoclastic bone erosion in Haversian remodeling sites of adult dog's rib
Jaworski, Z. F. G., & Lok, E. (1972) · Calcified Tissue International · doi:10.1007/bf02012540 · Cited by 90 · see citing works
Kinetics of osteoclasts and their nuclei in evolving secondary Haversian systems.
Jaworski, Z. F. G., Duck, B., & Sékaly, G. (1981) · PubMed · Cited by 89 · see citing works
Osteoblast Recruitment Routes in Human Cancellous Bone Remodeling
Kristensen, H. B., Andersen, T. L., Marcussen, N., Rolighed, L., & Delaissé, J. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.11.022 · Cited by 88 · see citing works
Self-citationAbdelgawad, M. E., Delaisse, J.-M., Hinge, M., Jensen, P. R., Alnaimi, R. W., Rolighed, L., Engelholm, L. H., Marcussen, N., & Andersen, T. L. (2016) · Histochemistry and Cell Biology · doi:10.1007/s00418-016-1414-y · Cited by 76 · see citing works
Self-citationLotinun, S., Sibonga, J. D., & Turner, R. T. (2002) · Endocrine · doi:10.1385/endo:17:1:29 · Cited by 69 · see citing works
Observations on Two Types of Resorption Cavities in Human Lamellar Cortical Bone
Jaworski, Z. F. G., Meunier, P. J., & Frost, H. M. (1972) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-197203000-00048 · Cited by 60 · see citing works
Abdelgawad, M. E., Søe, K., Andersen, T. L., Merrild, D. M. H., Christiansen, P., Kjærsgaard‐Andersen, P., & Delaissé, J. (2014) · Bone · doi:10.1016/j.bone.2014.07.012 · Cited by 58 · see citing works
Self-citationJensen, P. R., Andersen, T. L., Hauge, E., Bollerslev, J., & Delaissé, J. (2014) · Bone · doi:10.1016/j.bone.2014.12.004 · Cited by 57 · see citing works
Self-citationUpregulation of human heme oxygenase gene expression by Ets-family proteins
Deramaudt, B. M. J. ‐., Rémy, P., & Abraham, N. G. (1999) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(19990301)72:3 · Cited by 55 · see citing works
Study of cell kinetics within evolving secondary Haversian systems.
Jaworski, Z. F. G., & Hooper, C. (1980) · PubMed · Cited by 41 · see citing works
Morphometry of bone resorption: Introduction and overview
PARFITT, A. M. (1993) · Bone · doi:10.1016/8756-3282(93)90176-b · Cited by 40 · see citing works
Andersen, T. L., Hauge, E., Rolighed, L., Bollerslev, J., Kjærsgaard‐Andersen, P., & Delaissé, J. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.12.005 · Cited by 37 · see citing works
Self-citationBuenzli, P. R., Jeon, J., Pivonka, P., Smith, D. W., & Cummings, P. T. (2011) · Bone · doi:10.1016/j.bone.2011.10.021 · Cited by 37 · see citing works
Pratt, I. V., Belev, G. S., Zhu, N., Chapman, D., & Cooper, D. M. L. (2014) · Physics in Medicine and Biology · doi:10.1088/0031-9155/60/1/211 · Cited by 33 · see citing works
Morphological and Functional Features of Clasts in Low Phosphate, Vitamin D-Deficiency Rickets
Nordahl, J., Hollberg, K., Mengarelli-Widholm, S., Andersson, G. N., & Reinholt, F. P. (2000) · Calcified Tissue International · doi:10.1007/s002230001151 · Cited by 25 · see citing works
[Boring of the Haversian canals].
Dhem, A. (1966) · PubMed · Cited by 7 · see citing works
Does collagen trigger migration of reversal cells into vacated bone resorption lacunae?
Abdelgawad, M. E., Søe, K., Engelholm, L. H., Kjærsgaard‐Andersen, P., Behrendt, N., & Delaissé, J. (2012) · University of Southern Denmark Research Portal (University of Southern Denmark) · Cited by 2 · see citing works
Self-citationAndreasen, C. M., Delaissé, J., van der Eerden, B. C. J., Birkenhäger-Frenkel, D. H., van Leeuwen, J. P. T. M., Ding, M. L., & Andersen, T. L. (2016) · University of Southern Denmark Research Portal (University of Southern Denmark) · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 4
- Baron R. Importance of the intermediate phases between resorption and formation in the measurement and understanding of the bone remodeling sequence. In: Meunier PJ, editor. Bone histo- morphometry: second international workshop Lyon. Toulouse: Armour Montagu; 1977. p. 179-83.
- Aubin JE. Osteoprogenitor cell frequency in rat bone marrow stromal populations: role for heterotypic cell-cell interactions in osteoblast differentiation. J Cell Biochem. 1999;72(3):396-410.
- Parfitt AM. The physiologic and clinical significance of bone histomorphometric data. In: Recker RR, editor. Bone histomorphometry: techniques and interpretation. Boca Raton: CRC Press; 1983. p. 143-223.
- Baron R, Vignery A, Lang R. Reversal phase and osteopenia: defective coupling of resorption to formation in the pathogene- sis of osteoporosis. In: Deluca HF, Frost HM, Jee WSS, Johnston CC, Parfitt AM, editors. Osteoporosis: recent advances in pathogenesis and treatment. Baltimore: University Park Press; 1980. p. 311-20.
Cited by
Sorted by citations
Bone remodeling: an operational process ensuring survival and bone mechanical competence
Bolamperti, S., Villa, I., & Rubinacci, A. (2022) · Bone Research · doi:10.1038/s41413-022-00219-8 · Cited by 482 · see citing works
The Osteosarcoma Microenvironment: A Complex but Targetable Ecosystem
Corre, I., Verrecchia, F., Crenn, V., Rédiní, F., & Trichet, V. (2020) · Cells · doi:10.3390/cells9040976 · Cited by 475 · see citing works
Osteoclasts recycle via osteomorphs during RANKL-stimulated bone resorption
McDonald, M. M., Khoo, W. H., Ng, P. Y., Xiao, Y., Zamerli, J., Thatcher, P., Kyaw, W., Pathmanandavel, K., Grootveld, A. K., Moran, I., et al. (2021) · Cell · doi:10.1016/j.cell.2021.02.002 · Cited by 433 · see citing works
A network of trans-cortical capillaries as mainstay for blood circulation in long bones
Grüneboom, A., Hawwari, I., Weidner, D., Culemann, S., Müller, S., Henneberg, S., Brenzel, A., Merz, S. F., Bornemann, L., Zec, K., et al. (2018) · Nature Metabolism · doi:10.1038/s42255-018-0016-5 · Cited by 301 · see citing works
Osteoclasts Provide Coupling Signals to Osteoblast Lineage Cells Through Multiple Mechanisms
Sims, N. A., & Martin, T. J. (2020) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021119-034425 · Cited by 286 · see citing works
Weivoda, M. M., Chew, C. K., Monroe, D. G., Farr, J. N., Atkinson, E. J., Geske, J. R., Eckhardt, B., Thicke, B., Ruan, M., Tweed, A. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-14003-6 · Cited by 230 · see citing works
Self-citationTargeting strategies for bone diseases: signaling pathways and clinical studies
Xu, H., Wang, W., Liu, X., Huang, W. H., Chen, Z., Xu, Y., Yang, H., Bai, J., & Geng, D. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01467-8 · Cited by 173 · see citing works
Re-thinking the bone remodeling cycle mechanism and the origin of bone loss
Delaisse, J.-M., Andersen, T. L., Kristensen, H. B., Jensen, P. R., Andreasen, C. M., & Søe, K. (2020) · Bone · doi:10.1016/j.bone.2020.115628 · Cited by 152 · see citing works
Self-citationTencerova, M., Frost, M., Figeac, F., Nielsen, T., Ali, D., Lauterlein, J., Andersen, T. L., Haakonsson, A., Rauch, A., Madsen, J. S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.066 · Cited by 125 · see citing works
Self-citationBiological basis of bone strength: anatomy, physiology and measurement.
Hart, N. H., Newton, R. U., Tan, J., Rantalainen, T., Chivers, P., Siafarikas, A., & Nimphius, S. (2020) · PubMed Central · Cited by 135 · see citing works
Local Production of Osteoprotegerin by Osteoblasts Suppresses Bone Resorption
Cawley, K. M., Bustamante-Gomez, N. C., Guha, A. G., MacLeod, R. S., Xiong, J., Gubrij, I., Liu, Y., Mulkey, R., Palmieri, M., Thostenson, J. D., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108052 · Cited by 114 · see citing works
Osteon: Structure, Turnover, and Regeneration
Chang, B., & Liu, X. (2021) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2020.0322 · Cited by 114 · see citing works
Coupling factors involved in preserving bone balance
Kim, B.-J., & Koh, J.-M. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2981-y · Cited by 111 · see citing works
New Insights Into Osteoclast Biology
McDonald, M. M., Kim, A. S., Mulholland, B. S., & Rauner, M. (2021) · JBMR Plus · doi:10.1002/jbm4.10539 · Cited by 116 · see citing works
The origins and roles of osteoclasts in bone development, homeostasis and repair
Yahara, Y., Nguyen, T., Ishikawa, K., Kamei, K., & Alman, B. A. (2022) · Development · doi:10.1242/dev.199908 · Cited by 107 · see citing works
The critical interplay between bone resorbing and bone forming cells
Lerner, U. H., Kindstedt, E., & Lundberg, P. (2019) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.13051 · Cited by 99 · see citing works
Skeleton-vasculature chain reaction: a novel insight into the mystery of homeostasis
Chen, M., Li, Y., Huang, X., Gu, Y., Li, S., Yin, P., Zhang, L., & Tang, P. (2021) · Bone Research · doi:10.1038/s41413-021-00138-0 · Cited by 95 · see citing works
Destroy to Rebuild: The Connection Between Bone Tissue Remodeling and Matrix Metalloproteinases
Hardy, E., & Fernández-Patrón, C. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00047 · Cited by 85 · see citing works
Bisphosphonates impair the onset of bone formation at remodeling sites
Jensen, P. R., Andersen, T. L., Chavassieux, P., Roux, J.-P., & Delaissé, J. (2021) · Bone · doi:10.1016/j.bone.2021.115850 · Cited by 83 · see citing works
Self-citationRecent Advances in Osteoclast Biological Behavior
Sun, Y., Li, J., Xie, X., Gu, F., Sui, Z., Zhang, K., & Yu, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.788680 · Cited by 81 · see citing works
Ma, J., Lin, X., Chen, C., Li, S., Zhang, S., Chen, Z., Li, D., Zhao, F., Yang, C., Yin, C., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgz300 · Cited by 80 · see citing works
Xie, Y., Pan, M., Gao, Y., Zhang, L., Ge, W., & Tang, P. (2019) · Cell & Bioscience · doi:10.1186/s13578-019-0369-9 · Cited by 75 · see citing works
Sayilekshmy, M., Hansen, R. B., Delaissé, J., Rolighed, L., Andersen, T. L., & Heegaard, A. (2019) · Scientific Reports · doi:10.1038/s41598-019-41779-w · Cited by 73 · see citing works
Self-citationEl-Masri, B. M., Andreasen, C. M., Laursen, K. S., Kofod, V. B., Borggaard, X. G., Nielsen, M. H., Thomsen, J. S., Brüel, A., Sørensen, M. S., Hansen, L. J., et al. (2024) · Bone Research · doi:10.1038/s41413-024-00362-4 · Cited by 72 · see citing works
Self-citationAndreasen, C. M., Delaissé, J., van der Eerden, B. C. J., van Leeuwen, J. P. T. M., Ding, M. L., & Andersen, T. L. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3354 · Cited by 70 · see citing works
Self-citationStockhausen, K. E., Qwamizadeh, M., Wölfel, E. M., Hemmatian, H., Fiedler, I. A. K., Flenner, S., Longo, E., Amling, M., Greving, I., Ritchie, R. O., et al. (2021) · ACS Nano · doi:10.1021/acsnano.0c04786 · Cited by 70 · see citing works
Bone Hierarchical Structure: Heterogeneity and Uniformity
Rodríguez-Palomo, A., Østergaard, M., & Birkedal, H. (2023) · Advanced Functional Materials · doi:10.1002/adfm.202307026 · Cited by 72 · see citing works
de Molon, R. S., Vernal, R., Oliveira, G. E., Steffens, J. P., Ervolino, E., Theodoro, L. H., van den Beucken, J. J. J. P., & Tetradis, S. (2026) · Bone Research · doi:10.1038/s41413-025-00478-1 · Cited by 83 · see citing works
Moldovan, L.-I., Hansen, T. B., Venø, M. T., Okholm, T. L. H., Andersen, T. L., Hager, H., Iversen, L., Kjems, J., Johansen, C., & Kristensen, L. S. (2019) · BMC Medical Genomics · doi:10.1186/s12920-019-0616-2 · Cited by 64 · see citing works
Self-citationLi, X., Dai, B., Guo, J., Zhu, Y., Xu, J., Xu, S., Yao, Z., Chang, L., Li, Y., He, X. M., et al. (2022) · ACS Nano · doi:10.1021/acsnano.2c04747 · Cited by 63 · see citing works
GIP reduces osteoclast activity and improves osteoblast survival in primary human bone cells
Hansen, M. S., Søe, K., Christensen, L. L., Fernandez-Guerra, P., Hansen, N. W., Wyatt, R. A., Martin, C., Hardy, R. S., Andersen, T. L., Olesen, J. B., et al. (2023) · European Journal of Endocrinology · doi:10.1093/ejendo/lvac004 · Cited by 62 · see citing works
Self-citationVind, A., Wu, Z., Firdaus, M. J., Snieckute, G., Toh, G. A., Jessen, M., Martı́nez, J. F., Haahr, P., Andersen, T. L., Blasius, M., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.10.044 · Cited by 63 · see citing works
Self-citationFigeac, F., Tencerova, M., Ali, D., Andersen, T. L., Appadoo, D. R. C., Kerckhofs, G., Ditzel, N., Kowal, J., Rauch, A., & Kassem, M. (2022) · Stem Cells · doi:10.1093/stmcls/sxab011 · Cited by 50 · see citing works
Self-citationSøe, K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207717 · Cited by 58 · see citing works
Self-citationBone Biomineral Properties Vary across Human Osteonal Bone
Wittig, N. K., Palle, J., Østergaard, M., Frølich, S., Birkbak, M. E., Spiers, K., Garrevoet, J., & Birkedal, H. (2019) · ACS Nano · doi:10.1021/acsnano.9b05535 · Cited by 51 · see citing works
Cortical Bone Porosity in Rabbit Models of Osteoporosis
Harrison, K. D., Hiebert, B. D., Panahifar, A., Andronowski, J. M., Ashique, A. M., King, G. A., Arnason, T., Swekla, K. J., Pivonka, P., & Cooper, D. M. L. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4124 · Cited by 52 · see citing works
Adami, G., Pedrollo, E., Rossini, M., Fassio, A., Braga, V., Pasetto, E., Pollastri, F., Benini, C., Viapiana, O., & Gatti, D. (2024) · JBMR Plus · doi:10.1093/jbmrpl/ziae016 · Cited by 45 · see citing works
KIAA1199 is a secreted molecule that enhances osteoblastic stem cell migration and recruitment
Chen, L., Shi, K., Andersen, T. L., Qiu, W., & Kassem, M. S. (2019) · Cell Death and Disease · doi:10.1038/s41419-018-1202-9 · Cited by 41 · see citing works
Self-citationChavassieux, P., & Chapurlat, R. D. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.907914 · Cited by 45 · see citing works
RSPO3 is important for trabecular bone and fracture risk in mice and humans
Nilsson, K. H., Henning, P., Shahawy, M. E., Nethander, M., Andersen, T. L., Ejersted, C., Wu, J., Gustafsson, K. L., Koskela, A., Tuukkanen, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25124-2 · Cited by 39 · see citing works
Self-citationChen, L., Shi, K., Ditzel, N., Qiu, W., Figeac, F., Nielsen, L. H. D., Tencerová, M., Kowal, J. M., Ding, M. L., Andreasen, C. M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37651-1 · Cited by 39 · see citing works
Self-citationLarge cortical bone pores in the tibia are associated with proximal femur strength
Iori, G., Schneider, J., Reisinger, A., Heyer, F. L., Peralta, L. M., Wyers, C. E., Gräsel, M., Barkmann, R., Glüer, C., van den Bergh, J. P., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0215405 · Cited by 39 · see citing works
Estimation of Cortical Bone Microstructure From Ultrasound Backscatter
Iori, G., Du, J., Hackenbeck, J., Kilappa, V., & Raum, K. (2020) · IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control · doi:10.1109/tuffc.2020.3033050 · Cited by 37 · see citing works
Intracortical Bone Mechanics Are Related to Pore Morphology and Remodeling in Human Bone
Bakalova, L., Andreasen, C. M., Thomsen, J. S., Brüel, A., Hauge, E., Kiil, B. J., Delaissé, J., Andersen, T. L., & Kersh, M. E. (2018) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3561 · Cited by 34 · see citing works
Self-citationBrun, J., Andreasen, C. M., Ejersted, C., Andersen, T. L., Caverzasio, J., & Thouverey, C. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4150 · Cited by 34 · see citing works
Self-citation3D analysis of the osteonal and interstitial tissue in human radii cortical bone
Gauthier, R., Follet, H., Olivier, C., Mitton, D., & Peyrin, F. (2019) · Bone · doi:10.1016/j.bone.2019.07.028 · Cited by 26 · see citing works
Alias, M. A., & Buenzli, P. R. (2018) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-018-1031-x · Cited by 28 · see citing works
Assembling the Puzzle Pieces. Insights for in Vitro Bone Remodeling
Krasnova, O. A., & Neganova, I. E. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10558-6 · Cited by 26 · see citing works
Andreasen, C. M., Delaissé, J., van der Eerden, B. C. J., van Leeuwen, J. P. T. M., Ding, M. L., & Andersen, T. L. (2018) · Bone · doi:10.1016/j.bone.2018.09.011 · Cited by 26 · see citing works
Self-citationBeyond resorption: osteoclasts as drivers of bone formation
Xiang, Q., Li, L., Ji, W., Gawlitta, D., Walboomers, X. F., & van den Beucken, J. J. J. P. (2024) · Cell Regeneration · doi:10.1186/s13619-024-00205-x · Cited by 29 · see citing works
The Cells of Bone and Their Interactions
Ansari, N., & Sims, N. A. (2019) · Handbook of experimental pharmacology · doi:10.1007/164_2019_343 · Cited by 27 · see citing works
Borggaard, X. G., Nielsen, M. H., Delaissé, J., Andreasen, C. M., & Andersen, T. L. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.896841 · Cited by 25 · see citing works
Self-citationHarrison, K. D., Sales, E., Hiebert, B. D., Panahifar, A., Zhu, N., Arnason, T., Swekla, K. J., Pivonka, P., Chapman, D., & Cooper, D. M. L. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4700 · Cited by 24 · see citing works
Walle, M., Gabel, L., Whittier, D. E., Liphardt, A., Hulme, P. A., Heer, M. A., Zwart, S. R., Smith, S. M., Sibonga, J. D., & Boyd, S. K. (2024) · Science Advances · doi:10.1126/sciadv.adq3632 · Cited by 23 · see citing works
Catabolic activity of osteoblast lineage cells contributes to osteoclastic bone resorption in vitro
Pirapaharan, D. C., Olesen, J. B., Andersen, T. L., Christensen, S. B., Kjærsgaard‐Andersen, P., Delaissé, J., & Søe, K. (2019) · Journal of Cell Science · doi:10.1242/jcs.229351 · Cited by 22 · see citing works
Self-citationModelling cell guidance and curvature control in evolving biological tissues
Hegarty-Cremer, S. G. D., Simpson, M. J., Andersen, T. L., & Buenzli, P. R. (2021) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2021.110658 · Cited by 22 · see citing works
Self-citationA Critical Role of the Bone Marrow Envelope in Human Bone Remodeling
Andersen, T. L., Jensen, P. R., Sikjær, T., Rejnmark, L., Ejersted, C., & Delaissé, J. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4815 · Cited by 20 · see citing works
Self-citationAndreasen, C. M., Bakalova, L., Brüel, A., Hauge, E., Kiil, B. J., Delaissé, J., Kersh, M. E., Thomsen, J. S., & Andersen, T. L. (2019) · Bone · doi:10.1016/j.bone.2019.115127 · Cited by 20 · see citing works
Self-citationYao, Z., Chen, P., Fan, L., Chen, P., Zhang, X., & Yu, B. (2021) · The FASEB Journal · doi:10.1096/fj.202002808rr · Cited by 19 · see citing works
Osteoclast-derived coupling factors: origins and state-of-play Louis V Avioli lecture, ASBMR 2023
Sims, N. A. (2024) · Journal of Bone and Mineral Research · doi:10.1093/jbmr/zjae110 · Cited by 18 · see citing works
Tethering Formation to Resorption: Reversal Revisited
Dempster, D. W. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3169 · Cited by 18 · see citing works
Andreasen, C. M., El-Masri, B. M., MacDonald, B., Laursen, K. S., Nielsen, M. H., Thomsen, J. S., Delaissé, J., & Andersen, T. L. (2023) · Bone · doi:10.1016/j.bone.2023.116787 · Cited by 16 · see citing works
Self-citationMaggiano, I. S., Maggiano, C. M., & Cooper, D. M. L. (2020) · Micron · doi:10.1016/j.micron.2020.102955 · Cited by 16 · see citing works
Closing cones create conical lamellae in secondary osteonal bone
Doube, M. (2022) · Royal Society Open Science · doi:10.1098/rsos.220712 · Cited by 15 · see citing works
Loundagin, L. L., Harrison, K. D., Wei, X., & Cooper, D. M. L. (2023) · Bone · doi:10.1016/j.bone.2023.116960 · Cited by 14 · see citing works
Loundagin, L. L., & Cooper, D. (2022) · European Cells and Materials · doi:10.22203/ecm.v043a15 · Cited by 14 · see citing works
Alendronate prolongs the reversal-resorption phase in human cortical bone remodeling
Borggaard, X. G., Roux, J.-P., Delaissé, J., Chavassieux, P., Andreasen, C. M., & Andersen, T. L. (2022) · Bone · doi:10.1016/j.bone.2022.116419 · Cited by 14 · see citing works
Self-citationFIBCD1 is an endocytic GAG receptor associated with a novel neurodevelopmental disorder
Fell, C. W., Hagelkrüys, A., Cicvaric, A., Horrer, M., Liu, L., Li, J. S. S., Stadlmann, J., Polyansky, A. A., Mereiter, S., Tejada, M. A., et al. (2022) · EMBO Molecular Medicine · doi:10.15252/emmm.202215829 · Cited by 12 · see citing works
Self-citationSeeler, S., Moldovan, L.-I., Bertelsen, T., Hager, H., Iversen, L., Johansen, C., Kjems, J., & Kristensen, L. S. (2022) · PLoS ONE · doi:10.1371/journal.pone.0275219 · Cited by 12 · see citing works
Nielsen, S. S. R., Pedersen, J. A. Z., Sharma, N., Wasehuus, P. K., Hansen, M. S., Møller, A. M. J., Borggaard, X. G., Rauch, A., Frost, M., Søndergaard, T. E., et al. (2024) · Bone · doi:10.1016/j.bone.2024.117035 · Cited by 13 · see citing works
Self-citationIori, G., Schneider, J., Reisinger, A., Heyer, F. L., Peralta, L. M., Wyers, C. E., Glüer, C., van den Bergh, J. P., Pahr, D. H., & Raum, K. (2020) · Bone · doi:10.1016/j.bone.2020.115446 · Cited by 12 · see citing works
Osteocyte- and late osteoblast-derived NOTUM reduces cortical bone mass in mice
Nilsson, K. H., Henning, P., Shahawy, M. E., Wu, J., Koskela, A., Tuukkanen, J., Perret, C., Lerner, U. H., Ohlsson, C., & Movérare‐Skrtic, S. (2021) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00565.2020 · Cited by 12 · see citing works
Hirano, F., Okuma, K. F., Zenke, Y., Menuki, K., Ohnishi, H., Fukuda, F., Sakai, A., Yamamoto, N., Shimakura, T., Sano, H., et al. (2021) · Bone Reports · doi:10.1016/j.bonr.2021.101091 · Cited by 12 · see citing works
Kottmann, V., Nienhaus, M., Drees, P., Gercek, E., & Ritz, U. (2026) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2026.189551 · Cited by 14 · see citing works
Significance of Reversal-Resorption Phase in Bone Loss
Andersen, T. L., Delaissé, J., Thomsen, J. S., & Andreasen, C. M. (2021) · Springer eBooks · doi:10.1007/978-981-16-5613-2_7 · Cited by 11 · see citing works
Self-citationLamarche, B. A., Thomsen, J. S., Andreasen, C. M., Lievers, W. B., & Andersen, T. L. (2022) · Bone · doi:10.1016/j.bone.2022.116399 · Cited by 11 · see citing works
Self-citationFrost, M., Rahbek, E. T., Ejersted, C., Høilund‐Carlsen, P. F., Bygum, A., Thomsen, J. S., Andreasen, C. M., Andersen, T. L., & Frederiksen, A. L. (2020) · Bone · doi:10.1016/j.bone.2020.115313 · Cited by 11 · see citing works
Self-citationDeng, J., Zhang, Y.-N., Bai, R., Yu, T., Zhao, Y., Liu, H., Zhang, Y.-F., Xu, T., & Han, B. (2025) · Progress in Orthodontics · doi:10.1186/s40510-024-00548-w · Cited by 10 · see citing works
Pathophysiology of bone remodelling cycle: Role of immune system and lipids
Parolini, C. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.116844 · Cited by 10 · see citing works
Diaz‐delCastillo, M., Gundesen, M. T., Andersen, C. W., Nielsen, A. L., Møller, H. E. H., Vinholt, P. J., Asmussen, J. T., Kristensen, I. B., Nyvold, C. G., Abildgaard, N., et al. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4807 · Cited by 10 · see citing works
Self-citationCooper, D. M. L., Harrison, K. D., Hiebert, B. D., King, G. A., Panahifar, A., Zhu, N., Swekla, K. J., Pivonka, P., Chapman, D., & Arnason, T. (2023) · Bone · doi:10.1016/j.bone.2023.116864 · Cited by 10 · see citing works
Bone loss markers in the earliest Pacific Islanders
Miszkiewicz, J. J., Valentin, F., Vrahnas, C., Sims, N. A., Vongsvivut, J. P., Tobin, M. J., & Clark, G. (2021) · Scientific Reports · doi:10.1038/s41598-021-83264-3 · Cited by 10 · see citing works
The mineralization of osteonal cement line depends on where the osteon is formed
Cantamessa, A., Blouin, S., Rummler, M., Berzlanovich, A. M., Weinkamer, R., Hartmann, M. A., & Ruffoni, D. (2025) · JBMR Plus · doi:10.1093/jbmrpl/ziaf114 · Cited by 9 · see citing works
Takakura, A., Sato, T., Lee, J., Hirano, K., Takao-Kawabata, R., Ishizuya, T., & Iimura, T. (2022) · Scientific Reports · doi:10.1038/s41598-022-20793-5 · Cited by 9 · see citing works
HYBID in osteoarthritis: Potential target for disease progression
Zheng, S., An, S., Luo, Y., Vithran, D. T. A., Yang, S., Lu, B., Deng, Z., & Li, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115043 · Cited by 9 · see citing works
Matrix first, minerals later: fine-tuned dietary phosphate increases bone formation in zebrafish
Cotti, S., Biagio, C. D., Huysseune, A., Koppe, W., Forlino, A., & Witten, P. E. (2024) · JBMR Plus · doi:10.1093/jbmrpl/ziae081 · Cited by 9 · see citing works
Coupling of bone formation and resorption
Sims, N. A., & Martin, T. J. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-814841-9.00010-5 · Cited by 9 · see citing works
Christiansen, P. V. D., Andreasen, C. M., El-Masri, B. M., Laursen, K. S., Delaissé, J., & Andersen, T. L. (2023) · Bone · doi:10.1016/j.bone.2023.116896 · Cited by 8 · see citing works
Self-citationHenning, P., Movérare‐Skrtic, S., Westerlund, A., de Souza, P. P. C., Marcelino, T. F., Nilsson, K. H., Shahawy, M. E., Ohlsson, C., & Lerner, U. H. (2021) · Journal of Inflammation Research · doi:10.2147/jir.s323435 · Cited by 8 · see citing works
Fujihara, R., Mashiba, T., Shingo, Y., Komatsubara, S., Iwata, K., Takao-Kawabata, R., & Yamamoto, T. (2019) · Bone · doi:10.1016/j.bone.2019.01.006 · Cited by 8 · see citing works
Jensen, L. D., El-Masri, B. M., Ejersted, C., Andreasen, C. M., Thomsen, L. K., Thomsen, J. S., Andersen, T. L., & Hansen, S. G. (2023) · Bone Reports · doi:10.1016/j.bonr.2023.101703 · Cited by 7 · see citing works
Self-citationVascular study of decellularized porcine long bones: Characterization of a tissue engineering model
Evrard, R., Manon, J., Rafferty, C., Fievé, L., Cornu, O., Kirchgesner, T., Lecouvet, F. E., Schubert, T., & Lengelé, B. (2024) · Bone · doi:10.1016/j.bone.2024.117073 · Cited by 7 · see citing works
Elongation of the Long Bones in Humans by the Growth Plates
Hunziker, E. B. (2018) · Nestlé Nutrition Institute Workshop series · doi:10.1159/000486489 · Cited by 7 · see citing works
Schlosser, A. G., Pilecki, B., Allen, C., Benest, A. V., Lynch, A. P., Hua, J., Ved, N., Blackley, Z., Andersen, T. L., Hennig, D., et al. (2025) · Molecular Therapy · doi:10.1016/j.ymthe.2025.01.038 · Cited by 6 · see citing works
Self-citationCathepsin K inhibitors promote osteoclast-osteoblast communication and engagement of osteogenesis
Panwar, P., Olesen, J. B., Delaissé, J., Søe, K., & Brömme, D. (2025) · JBMR Plus · doi:10.1093/jbmrpl/ziaf079 · Cited by 5 · see citing works
Self-citationChristiansen, P. V. D., Sikjær, T., Andreasen, C. M., Thomsen, J. S., Brüel, A., Hauge, E., Delaissé, J., Rejnmark, L., & Andersen, T. L. (2023) · JBMR Plus · doi:10.1002/jbm4.10829 · Cited by 5 · see citing works
Self-citationHegarty-Cremer, S. G. D., Borggaard, X. G., Andreasen, C. M., van der Eerden, B. C. J., Simpson, M. J., Andersen, T. L., & Buenzli, P. R. (2024) · Bone · doi:10.1016/j.bone.2023.116998 · Cited by 6 · see citing works
Self-citationWang, W., Azar, T., Tseng, W., Pei, S., Zhou, Y., Jiang, X., Dyment, N. A., & Liu, X. S. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4704 · Cited by 5 · see citing works
Reflecting on Some Discoveries of 40 Years and Their Outcomes
Martin, T. J. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3282 · Cited by 5 · see citing works
Thomsen, L. K., Christiansen, P. V. D., Andreasen, C. M., & Andersen, T. L. (2025) · Osteoporosis International · doi:10.1007/s00198-025-07612-z · Cited by 4 · see citing works
Self-citation
- Authors
- Lassen, N. E., Andersen, T. L., Pløen, G. G., Søe, K., Hauge, E. M., Harving, S., Eschen, G. E. T., & Delaisse, J.-M.
- Affiliations
- University of Southern Denmark (DK)
- Aarhus University (DK)
- Aalborg University Hospital (DK)
- Department of Plastic SurgeryAarhus University HospitalAarhusDenmark
- Clinical Cell BiologyInstitute of Regional Health ResearchUniversity of Southern DenmarkVejle/Lillebaelt HospitalVejleDenmark
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-02-08
- Volume
- 32
- Issue
- 7
- Pages
- 1395-1405
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- OpenAlex
- W2586325787
- Cited by
- 152
- References
- 44
- Citations by year
- 2026: 10 · 2025: 19 · 2024: 16 · 2023: 19 · 2022: 17 · 2021: 21 · 2020: 20 · 2019: 20 · 2018: 6 · 2017: 3
- FWCI
- 5.48
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Journal of Bone and Mineral Research (publishedVersion)
- PubMed (publishedVersion)
- VBN Forskningsportal (Aalborg Universitet) (publishedVersion, other-oa)
- Scopus (Elsevier) (submittedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, other-oa)
- Funders
- Velux Foundation (VELUX34368)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Alkaline Phosphatase Research Studies
- Keywords
- bone remodeling, basic multicellular unit, bone resorption, bone formation, osteoprogenitor cells, osteoclasts, osteoblasts, Haversian canals, long bones, canal diameter, 3D reconstruction
- MeSH terms
- Bone Resorption, Humans, Osteoclasts, Bone Remodeling
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
