Uncoupling of bone metabolism in rheumatoid arthritis patients with or without joint destruction: assessment with serum type I collagen breakdown products.
Abstract
In this study we investigate bone metabolism in patients with rheumatoid arthritis (RA), with or without joint destruction, using serum biochemical markers of bone turnover. Three hundred eighteen patients (disease duration >2 years; mean 9 years) were divided into those with joint destruction, that is, with Larsen wrist X-ray index > or =2 (n = 173) and those without joint destruction, that is, with Larsen wrist X-ray index <2 (n = 145). Bone formation was assessed by serum osteocalcin levels and bone resorption by a new assay for serum type I collagen C-telopeptide breakdown products (serum CTX). Osteocalcin levels were significantly lower in both destructive (-17%) and nondestructive (-22%) groups compared with 319 healthy gender- and age-matched control subjects (p < 0.001 for both groups), but were similar in the two arthritis groups. CTX levels were increased in patients with destructive arthritis compared with controls (+35%, p < 0.001), but were not different between those with nondestructive arthritis and controls. In patients with joint destruction, decreased bone formation rate was amplified in those on steroids (n = 72) compared with nonusers (n = 101) as demonstrated by lower osteocalcin levels (p = 0.02). CTX levels, but not osteocalcin levels, were positively correlated with indices of disease activity and, moreover, of joint destruction (p < 0.002-0.0001). These results indicate that bone metabolism is uncoupled in patients with RA. Bone formation appears to be reduced both in patients with and without joint destruction, whereas resorption is increased only in patients with joint destruction in relation to disease activity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Systemic stimulation of bone resorption in RA patients is suggested by increases in circulating biochemical markers of bone resorption and increased osteoclastogenic potential of their bone marrow.
“Systemic stimulation of bone resorption in RA patients is suggested by increases in circulating biochemical markers of bone resorption (426) and increased osteoclastogenic potential of their bone marrow (426, 427).”
From Receptor Activator of Nuclear Factor κB Ligand and Osteoprotegerin Regulation of Bone Remodeling in Health and Disease (2008) · cites this paper as [426]
Cites
Arnett, F. C., Edworthy, S. M., Bloch, D. A., McShane, D. J., Fries, J. F., Cooper, N. S., Healey, L. A., Kaplan, S. R., Liang, M. H., Luthra, H. S., et al. (1988) · Arthritis & Rheumatism · doi:10.1002/art.1780310302 · Cited by 19,753 · see citing works
Revised Criteria for the Classification of Rheumatoid Arthritis
Arnett, F. C. (1990) · Orthopaedic Nursing · doi:10.1097/00006416-199003000-00011 · Cited by 7,742 · see citing works
THERAPEUTIC CRITERIA IN RHEUMATOID ARTHRITIS
Steinbrocker, O. (1949) · JAMA · doi:10.1001/jama.1949.02900430001001 · Cited by 2,898 · see citing works
Radiographic Evaluation of Rheumatoid Arthritis and Related Conditions by Standard Reference Films
Larsen, A., Dale, K., & Eek, M. (1977) · Acta Radiologica Diagnosis · doi:10.1177/028418517701800415 · Cited by 1,835 · see citing works
Bertolini, D. R., Nedwin, G. E., Bringman, T. S., Smith, D. D., & Mundy, G. R. (1986) · Nature · doi:10.1038/319516a0 · Cited by 1,425 · see citing works
Ritchie, D. M., Boyle, J. A., Mcinnes, J. M., Jasani, M. K., Dalakos, T. G., Grieveson, P., & Buchanan, W. W. (1968) · QJM · doi:10.1093/oxfordjournals.qjmed.a067150 · Cited by 1,350 · see citing works
Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis
Garnero, P., Sornay‐Rendu, E., Chapuy, M. C., & Delmas, P. D. (1996) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650110307 · Cited by 1,000 · see citing works
Self-citationThe Effect of Glucocorticoids on Joint Destruction in Rheumatoid Arthritis
Kirwan, J. R. (1995) · New England Journal of Medicine · doi:10.1056/nejm199507203330302 · Cited by 817 · see citing works
Hanson, D. A., Weis, M. A., Bollen, A., Maslan, S., Singer, F. R., & Eyre, D. W. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650071119 · Cited by 653 · see citing works
Generalised bone loss in patients with early rheumatoid arthritis.
GOUGH, A. (1994) · The Lancet · doi:10.1016/s0140-6736(94)91049-9 · Cited by 630 · see citing works
Risteli, J., Elomaa, I., Niemi, S., Novamo, A., & Risteli, L. (1993) · Clinical Chemistry · doi:10.1093/clinchem/39.4.635 · Cited by 621 · see citing works
Immunoassay for quantifying type I collagen degradation products in urine evaluated
Bonde, M., Qvist, P., Fledelius, C., Riis, B. J., & Christiansen, C. (1994) · Clinical Chemistry · doi:10.1093/clinchem/40.11.2022 · Cited by 323 · see citing works
[7] Collagen cross-linking amino acids
Eyre, D. R. (1987) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(87)44176-1 · Cited by 316 · see citing works
Robins, S. P., Woitge, H. W., Hesley, R., Ju, J., Seyedin, S. M., & Seibel, M. J. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650091019 · Cited by 316 · see citing works
Immunoassay for urinary pyridinoline: The new marker of bone resorption
Seyedin, S. M., Kung, V. T., Daniloff, Y., Hesley, R., Gomez, B., Nielsen, L. A., Rosen, H. N., & Zuk, R. F. (1993) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650080515 · Cited by 241 · see citing works
Characterization of immunoreactive forms of human osteocalcin generated in vivo and in vitro
Garnero, P., Grimaux, M., Seguin, P., & Delmas, P. D. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650090215 · Cited by 241 · see citing works
Self-citationMarked diurnal variation in urinary excretion of pyridinium cross-links in premenopausal women.
Schlemmer, A., Hassager, C., Jensen, S. B., et al. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.3.1740479 · Cited by 193 · see citing works
The effect of rheumatoid arthritis and steroid therapy on bone density in postmenopausal women
Hall, G. M., Spector, T. D., Griffin, A. J., Jawad, A. S. M., Hall, M., & Doyle, D. (1993) · Arthritis & Rheumatism · doi:10.1002/art.1780361105 · Cited by 190 · see citing works
Measurement of serum osteocalcin with a human-specific two-site immunoradiometric assay
Garnero, P., Grimaux, M., Demiaux, B., Préaudat, C., Seguin, P., & Delmas, P. D. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650071206 · Cited by 182 · see citing works
Self-citationThe effect of calcium supplementation on the circadian rhythm of bone resorption.
Blumsohn, A., Herrington, K. A., Hannon, R., et al. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.3.8077353 · Cited by 168 · see citing works
Interleukin-1 beta stimulates bone resorption and inhibits bone formation in vivo.
Nguyen, L., Dewhirst, F. E., Hauschka, P. V., et al. (1991) · PubMed · Cited by 164 · see citing works
ZWEI RONTGENOLOGISCH DIAGNOSTIZIERTE FALLE VON MILZARTERIENANEURYSMA
Safwenberg, O. (1937) · Acta Radiologica · doi:10.1177/028418513701800310 · Cited by 161 · see citing works
Bonde, M., Garnero, P., Fledelius, C., Qvist, P., Delmas, P. D., & Christiansen, C. (1997) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1997.12.7.1028 · Cited by 133 · see citing works
Self-citationMarkers of bone metabolism in postmenopausal women with rheumatoid arthritis
Hall, G. M., Spector, T. D., & Delmas, P. D. (1995) · Arthritis & Rheumatism · doi:10.1002/art.1780380705 · Cited by 113 · see citing works
Self-citationGough, A., Peel, N. F. A., Eastell, R., Holder, R. L., Lilley, J., & Emery, P. (1994) · Annals of the Rheumatic Diseases · doi:10.1136/ard.53.1.14 · Cited by 106 · see citing works
Lems, W. F., Gerrits, M. I., Jacobs, J. W. G., van Vugt, R. M., van Rijn, H. J. M., & Bijlsma, J. W. J. (1996) · Annals of the Rheumatic Diseases · doi:10.1136/ard.55.5.288 · Cited by 88 · see citing works
Black, D. A. K., Marabani, M., Sturrock, R. D., et al. (1989) · Annals of the Rheumatic Diseases · doi:10.1136/ard.48.8.641 · Cited by 88 · see citing works
Marked diurnal variation in urinary excretion of pyridinium cross-links in premenopausal women
Schlemmer, A. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.74.3.476 · Cited by 88 · see citing works
Hassager, C., Jensen, L. T., P�denphant, J., et al. (1994) · Calcified Tissue International · doi:10.1007/bf00316286 · Cited by 82 · see citing works
The effect of calcium supplementation on the circadian rhythm of bone resorption
Blumsohn, A. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.79.3.730 · Cited by 69 · see citing works
Lower mobility and markers of bone resorption in the elderly
Lips, P. T. A. M., van Ginkel, F. C., Netelenbos, J. C., Wiersinga, A., & van der Vijgh, W. J. F. (1990) · Bone and Mineral · doi:10.1016/0169-6009(90)90099-2 · Cited by 65 · see citing works
Mundy, G. R., Oyajobi, B. O., Gutierrez, G. E., Sterling, J. A. R., Padalecki, S. S., Elefteriou, F., & Zhao, M. (2008) · Elsevier eBooks · doi:10.1016/b978-012370544-0.50020-3 · Cited by 59 · see citing works
URINARY EXCRETION OF PYRIDINIUM CROSSLINKS OF COLLAGEN CORRELATED WITH JOINT DAMAGE IN ARTHRITIS
ASTBURY, C., Bird, H. A., McLaren, A., & Robins, S. P. (1994) · Lara D. Veeken · doi:10.1093/rheumatology/33.1.11 · Cited by 59 · see citing works
Bone turnover in non-steroid treated rheumatoid arthritis.
Compston, J. E., Vedi, S., Croucher, P. I., Garrahan, N. J., & O’Sullivan, M. (1994) · Annals of the Rheumatic Diseases · doi:10.1136/ard.53.3.163 · Cited by 56 · see citing works
Mellish, R. W. E., O’Sullivan, M., Garrahan, N. J., & Compston, J. E. (1987) · Annals of the Rheumatic Diseases · doi:10.1136/ard.46.11.830 · Cited by 50 · see citing works
Hakala, M., Aman, S., Luukkainen, R., et al. (1995) · Annals of the Rheumatic Diseases · doi:10.1136/ard.54.11.886 · Cited by 44 · see citing works
Kollerup, G., Hansen, M., & HØRSLEV-PETERSEN, K. (1994) · Lara D. Veeken · doi:10.1093/rheumatology/33.9.816 · Cited by 35 · see citing works
Lems, W. F., Jacobs, J. W. G., Brink, H. R. V. D., et al. (1993) · Lara D. Veeken · doi:10.1093/rheumatology/32.9.787 · Cited by 28 · see citing works
Bone remodeling in osteoporosis associated with rheumatoid arthritis
Kröger, H., Arnala, I., & Alhava, E. M. (1991) · Calcified Tissue International · doi:10.1007/bf02555104 · Cited by 26 · see citing works
Increased levels of urinary collagen crosslinks in females with rheumatoid arthritis
Spector, T. D., James, I., Hall, G. M., Thompson, P. W., Perrett, D. I., & Hart, D. J. (1993) · Clinical Rheumatology · doi:10.1007/bf02231535 · Cited by 26 · see citing works
Hein, G. E., Franke, S., Müller, U., et al. (1997) · Clinical Rheumatology · doi:10.1007/bf02247846 · Cited by 23 · see citing works
Increased type I collagen degradation in early rheumatoid arthritis.
Kotaniemi, A., Isomäki, H. A., Hakala, M., et al. (1994) · PubMed · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Kearns, A. E., Khosla, S., & Kostenuik, P. J. (2008) · Endocrine Reviews · doi:10.1210/er.2007-0014 · Cited by 824 · see citing works
Bone Turnover Markers in the Diagnosis and Monitoring of Metabolic Bone Disease
Greenblatt, M. B., Tsai, J. N., & Wein, M. N. (2017) · Clinical Chemistry · doi:10.1373/clinchem.2016.259085 · Cited by 376 · see citing works
- Authors
- Garnero, P., Jouvenne, P., Buchs, N., Delmas, P. D., & Miossec, P.
- Affiliations
- Inserm (FR)
- Corresponding author
- Garnero, P
- Venue
- Bone
- Publisher
- Elsevier BV
- Published
- 1999-04
- Volume
- 24
- Issue
- 4
- Pages
- 381-385
- ISSN
- 1873-2763 (ISSN-L)
- 8756-3282
- OpenAlex
- W1986316445
- Cited by
- 79
- References
- 42
- Citations by year
- 2026: 1 · 2025: 2 · 2022: 3 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 3 · 2014: 1 · 2013: 3 · 2012: 4
- FWCI
- 2.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Bone (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
- 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
- Keywords
- rheumatoid arthritis, bone metabolism, joint destruction, osteocalcin, bone turnover markers, corticosteroid therapy, disease activity
- MeSH terms
- Arthritis, Rheumatoid, Bone and Bones, Bone Resorption, Collagen, Evaluation Studies as Topic, Female, Humans, Joint Diseases, Male, Methotrexate, Middle Aged, Peptides, Steroids, Biomarkers, Osteocalcin, Antirheumatic Agents, Collagen Type I
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
