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Review Article| Volume 37, ISSUE 3, P365-386, August 2011

Is There a Place for Bone Turnover Markers in the Assessment of Osteoporosis and its Treatment?

  • Jean-Pierre Devogelaer
    Correspondence
    Corresponding author.
    Affiliations
    Division of Rheumatology and Rheumatology Unit, Department of Medicine, UCL 5390, Université Catholique de Louvain in Brussels, Saint-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels, Belgium
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  • Yves Boutsen
    Affiliations
    Division of Rheumatology, Department of Medicine, UCL 5390, Université Catholique de Louvain in Brussels, Saint-Luc University Hospital, and University Hospital in Mont-Godinne, Avenue Dr Therasse 1, B-5530 Yvoir, Belgium
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  • Damien Gruson
    Affiliations
    Departments of Laboratory Medicine and Clinical Biochemistry, Université Catholique de Louvain in Brussels, Saint-Luc University Hospital, Avenue Hippocrate 10F, B-1200 Brussels, Belgium
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  • Daniel Manicourt
    Affiliations
    Division of Rheumatology and Rheumatology Unit, Department of Medicine, UCL 5390, Université Catholique de Louvain in Brussels, Saint-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels, Belgium
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      References

        • Mulcahy L.E.
        • Taylor D.
        • Lee T.C.
        • et al.
        RANKL and OPG activity is regulated by injury size in networks of osteocyte-like cells.
        Bone. 2011; 48: 182-188
        • Parfitt A.M.
        What is the normal rate of bone remodeling?.
        Bone. 2004; 35: 1-3
        • Glover S.J.
        • Gall M.
        • Schoenborn-Kellenberger O.
        • et al.
        Establishing a reference interval for bone turnover markers in 637 healthy, young, premenopausal women from United Kingdom, France, Belgium, and the United States.
        J Bone Miner Res. 2009; 24: 389-397
        • Recker R.R.
        • Kimmel D.B.
        • Parfitt A.M.
        • et al.
        Static and tetracycline-based bone histomorphometric data from 34 normal postmenopausal females.
        J Bone Miner Res. 1988; 3: 133-144
        • Johnell O.
        • Oden A.
        • De Laet C.
        • et al.
        Biochemical indices of bone turnover and the assessment of fracture probability.
        Osteoporos Int. 2002; 13: 523-526
        • Consensus development conference
        Diagnosis, prophylaxis and treatment of osteoporosis.
        Am J Med. 1993; 94: 646-650
        • World Health Organization
        Assessment of fracture risk and its application to screening for postmenopausal osteoporosis.
        (Technical report – series n 843) WHO, Geneva (Switzerland)1994
        • Kanis J.A.
        • Devogelaer J.-P.
        • Gennari C.
        Practical guide for the use of bone mineral measurements in the assessment of treatment of osteoporosis: a position paper of the European Foundation for Osteoporosis and Bone Disease. On behalf of the Scientific Advisory Board and the Board of National Societies.
        Osteoporos Int. 1996; 6: 256-261
        • Kanis J.A.
        • Johnell O.
        • Oden A.
        • et al.
        FRAX™ and the assessment of fracture probability in men and women from the UK.
        Osteoporos Int. 2008; 19: 385-397
        • Marshall D.
        • Johnell O.
        • Wedel H.
        Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures.
        Br Med J. 1996; 312: 1254-1259
        • Kanis J.A.
        • Johansson H.
        • Oden A.
        • et al.
        The effects of a FRAX® revision for the USA.
        Osteoporos Int. 2010; 21: 35-40
        • Kanis J.A.
        • Johansson H.
        • Oden A.
        • et al.
        Guidance for the adjustment of FRAX according to the dose of glucocorticoids.
        Osteoporos Int. 2011; 22: 809-816
        • McClung M.R.
        • Geusens P.
        • Miller P.D.
        • et al.
        Effect of risedronate on the risk of hip fracture in elderly women. For the Hip Intervention Program Study Group.
        N Engl J Med. 2001; 344: 333-340
        • Siris E.C.
        • Chen Y.T.
        • Abbott T.A.
        • et al.
        Bone mineral density thresholds for pharmacological intervention to prevent fractures.
        Arch Intern Med. 2004; 164: 1108-1112
        • Garnero P.
        • Sornay-Rendu E.
        • Chapuy M.C.
        • et al.
        Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis.
        J Bone Miner Res. 1996; 11: 337-349
        • Devogelaer J.P.
        • Depresseux G.
        • Le Thi C.
        • et al.
        Seasonal variation in bone mineral content in postmenopausal women.
        in: Dequeker J. Geusens P. Wahner H.W. Bone mineral measurement by photon absorptiometry. Leuven University Press, Leuven (Belgium)1988: 225
        • Rapuri P.B.
        • Kinayamu H.K.
        • Gallagher J.C.
        • et al.
        Seasonal changes in calciotropic hormones, bone markers, and bone mineral density in elderly women.
        J Clin Endocrinol Metab. 2002; 87: 2024-2032
        • Storm D.
        • Eslin R.
        • Porter E.S.
        • et al.
        Calcium supplementation prevents seasonal bone loss and changes in biochemical markers of bone turnover in elderly New England women: a randomized placebo-controlled trial.
        J Clin Endocrinol Metab. 1998; 83: 3817-3825
        • Manios Y.
        • Moschonis G.
        • Trovas G.
        • et al.
        Changes in biochemical indexes of bone metabolism and bone mineral density after 12-mo dietary intervention program: the postmenopausal health study.
        Am J Clin Nutr. 2007; 86: 781-789
        • Bonjour J.P.
        • Brandolini-Bunlon M.
        • Boirie Y.
        • et al.
        Inhibition of none turnover by milk intake in postmenopausal women.
        Br J Nutr. 2008; 100: 866-874
        • Macdonald H.M.
        • Black A.J.
        • Aucott L.
        • et al.
        Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: a randomized controlled trial.
        Am J Clin Nutr. 2008; 88: 465-474
        • Macdonald H.M.
        • New S.A.
        • Golden M.H.
        • et al.
        Nutritional associations with bone loss during the menopausal transition: evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids.
        Am J Clin Nutr. 2004; 79: 155-165
        • Ivaska K.K.
        • Gerdhem P.
        • Akesson K.
        • et al.
        Effect of fracture on bone turnover markers: a longitudinal study comparing marker levels before and after injury in 113 elderly women.
        J Bone Miner Res. 2007; 22: 1155-1164
        • Marcus R.
        • Holloway L.
        • Wells B.
        • et al.
        The relationship of biochemical markers of bone turnover to bone density changes in postmenopausal women: results from the Postmenopausal Estrogen/Progestin Interventions (PEPI) trial.
        J Bone Miner Res. 1999; 14: 1583-1595
        • Chapuy M.C.
        • Schott A.M.
        • Garnero P.
        • et al.
        Healthy elderly French women living at home have secondary hyperparathyroidism and high bone turnover in winter (EPIDOS study group).
        J Clin Endocrinol Metab. 1996; 81: 1129-1133
        • Garnero P.
        • Hausherr E.
        • Chapuy M.C.
        • et al.
        Markers of bone resorption predict hip fracture in elderly women: the EPIDOS prospective study.
        J Bone Miner Res. 1996; 11: 1531-1538
        • Garnero P.
        • Sornay-Rendu E.
        • Claustrat B.
        • et al.
        Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study.
        J Bone Miner Res. 2000; 15: 1526-1536
        • Ivaska K.K.
        • Gerdhem P.
        • Vaananen H.K.
        • et al.
        Bone turnover markers and prediction of fracture: a prospective follow-up study of 1040 elderly women for a mean of 9 years.
        J Bone Miner Res. 2010; 25: 393-403
        • Sornay-Rendu E.
        • Munoz F.
        • Garnero P.
        • et al.
        Identification of osteopenic women at high risk of fracture: the OFELY study.
        J Bone Miner Res. 2005; 20: 1813-1819
        • Ross P.D.
        • Kress B.C.
        • Parson R.E.
        • et al.
        Serum bone alkaline phosphatase and calcaneus bone density predict fractures: a prospective study.
        Osteoporos Int. 2000; 11: 76-82
        • Szulc P.
        • Chapuy M.-C.
        • Meunier P.J.
        • et al.
        Serum undercarboxylated osteocalcin is a marker of the risk of hip fracture: a three year follow-up study.
        Bone. 1996; 5: 487-488
        • Vergnaud P.
        • Garnero P.
        • Meunier P.J.
        • et al.
        Undercarboxylated osteocalcin measured with a specific immunoassay predicts hip fracture in elderly women: the EPIDOS study.
        J Clin Endocrinol Metab. 1997; 82: 719-724
        • Chapurlat R.D.
        • Garnero P.
        • Breart G.
        • et al.
        Serum type 1 collagen breakdown products (serum CTX) predicts hip fracture in elderly women: the EPIDOS study.
        Bone. 2000; 27: 283-286
        • Szulc P.
        • Montella A.
        • Delmas P.D.
        High bone turnover is associated with accelerated bone loss but not with increased fracture risk in men aged 50 and over: the prospective MINOS study.
        Ann Rheum Dis. 2008; 67: 1249-1255
        • Chaitou A.
        • Boutroy S.
        • Vilayphiou N.
        • et al.
        Association between bone turnover rate and bone microarchitecture in men: the STRAMBO study.
        J Bone Miner Res. 2010; 25: 2313-2323
        • Alexopoulou O.
        • Jamart J.
        • Devogelaer J.P.
        • et al.
        Bone density and markers of bone remodeling in type 1 male diabetic patients.
        Diabetes Metab. 2006; 32: 453-458
        • Ivaska K.K.
        • Lenora J.
        • Gerdhem P.
        • et al.
        Serial assessment of serum bone metabolism markers identifies women with the highest rate of bone loss and osteoporosis risk.
        J Clin Endocrinol Metab. 2008; 93: 2622-2632
        • Dresner-Pollak R.
        • Parker R.A.
        • Poku M.
        • et al.
        Biochemical markers of bone turnover reflect femoral bone loss in elderly women.
        Calcif Tissue Int. 1996; 59: 328-333
        • Ross P.D.
        • Knowlton W.
        Rapid bone loss is associated with increased levels of biochemical markers.
        J Bone Miner Res. 1998; 13: 297-302
        • Garnero P.
        • Sornay-Rendu E.
        • Duboeuf F.
        • et al.
        Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study.
        J Bone Miner Res. 1999; 14: 1614-1621
        • Hansen M.A.
        • Overgaard K.
        • Riis B.J.
        • et al.
        Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 year study.
        Br Med J. 1991; 303: 961-964
        • Lenora J.
        • Ivaska K.K.
        • Obrant K.J.
        • et al.
        Prediction of bone loss using biochemical markers of bone turnover.
        Osteoporos Int. 2007; 18: 1297-1305
        • Rogers A.
        • Hannon R.A.
        • Eastell R.
        Biochemical markers as predictors of rates of bone loss after menopause.
        J Bone Miner Res. 2000; 15: 1398-1404
        • Devogelaer J.P.
        • Nagant de Deuxchaisnes C.
        Use of pamidronate in chronic and acute bone loss conditions.
        Medicina. 1997; 57: 101-108
        • Bauer D.C.
        • Garnero P.
        • Hochberg M.C.
        • et al.
        Pretreatment levels of bone turnover and the fracture efficacy of alendronate: the fracture intervention trial.
        J Bone Miner Res. 2006; 21: 292-299
        • Seibel M.J.
        • Naganathan V.
        • Barton I.
        • et al.
        Relationship between pretreatment bone resorption and vertebral fracture incidence in postmenopausal women treated with risedronate.
        J Bone Miner Res. 2004; 19: 323-329
        • Bauer D.C.
        • Black D.M.
        • Garnero P.
        • et al.
        Change in bone turnover and hip, non-spine, and vertebral fracture in alendronate-treated women: the Fracture Intervention Trial.
        J Bone Miner Res. 2004; 19: 1250-1258
        • Schousboe J.T.
        • Bauer D.C.
        • Nyman J.A.
        • et al.
        Potential for bone turnover markers to cost-effectively identify and select post-menopausal osteopenic women at high risk of fracture for bisphosphonate therapy.
        Osteoporos Int. 2007; 18: 201-210
        • Chen P.
        • Satterwhite J.H.
        • Licata A.A.
        • et al.
        Early changes in biochemical markers of bone formation predict BMD response to teriparatide in postmenopausal women with osteoporosis.
        J Bone Miner Res. 2005; 20: 962-970
        • Eastell R.
        • Chen P.
        • Saag K.G.
        • et al.
        Bone formation markers in patients with glucocorticoid-induced osteoporosis treated with teriparatide or alendronate.
        Bone. 2010; 46: 929-934
        • Burshell A.L.
        • Möricke R.
        • Correa-Rotter R.
        • et al.
        Correlations between biochemical markers of bone turnover and bone density responses in patients with glucocorticoid-induced osteoporosis treated with teriparatide or alendronate.
        Bone. 2010; 46: 935-939
        • Devogelaer J.P.
        • Adler R.A.
        • Recknor C.
        • et al.
        Baseline glucocorticoid dose and bone mineral density response with teriparatide or alendronate therapy in patients with glucocorticoid-induced osteoporosis.
        J Rheumatol. 2010; 37: 141-148
        • Harris S.T.
        • Watts N.B.
        • Genant H.K.
        • et al.
        Effects of risedronate treatment on vertebral and non-vertebral fractures in women with postmenopausal osteoporosis: a randomized controlled trial.
        JAMA. 1999; 282: 1344-1352
        • Eastell R.
        • Barton I.
        • Hannon R.A.
        • et al.
        Relationship of early changes in bone resorption to the reduction in fracture risk with risedronate.
        J Bone Miner Res. 2003; 18: 1051-1056
        • Delmas P.D.
        • Recker R.R.
        • Chesnut C.H.
        • et al.
        Daily and intermittent oral ibandronate normalize bone turnover and provide significant reduction in vertebral fracture risk: results from the BONE study.
        Osteoporos Int. 2004; 15: 792-798
        • Cummings S.R.
        • Karpf D.B.
        • Harris F.
        • et al.
        Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs.
        Am J Med. 2002; 112: 281-289
        • Bone H.G.
        • Hosking D.
        • Devogelaer J.P.
        • et al.
        • Alendronate Phase III Osteoporosis Treatment Study Group
        Ten years’ experience with alendronate for osteoporosis in postmenopausal women.
        N Engl J Med. 2004; 350: 1189-1199
        • Glover S.J.
        • Eastell R.
        • McCloskey E.V.
        • et al.
        Rapid and robust response of biochemical markers of bone formation to teriparatide therapy.
        Bone. 2009; 45: 1053-1058
        • Heaney R.P.
        • Watson P.
        Variability in the measured response of bone to teriparatide.
        Osteoporos Int. 2010; 22: 1703-1708
        • Zanchetta J.R.
        • Bogado C.E.
        • Ferretti J.L.
        • et al.
        Effects of teriparatide [recombinant human parathyroid hormone (1–34)] on cortical bone in postmenopausal women with osteoporosis.
        J Bone Miner Res. 2003; 18: 539-543
        • Black D.M.
        • Greenspan S.L.
        • Ensrud K.E.
        • et al.
        The effects of parathyroid hormone and alendronate alone or in combination in postmenopausal osteoporosis.
        N Engl J Med. 2003; 349: 1207-1215
        • Finkelstein J.S.
        • Wyland J.J.
        • Lee H.
        • et al.
        Effects of teriparatide, alendronate, or both in women with postmenopausal osteoporosis.
        J Clin Endocrinol Metab. 2010; 95: 1838-1845
        • Meunier P.J.
        • Roux C.
        • Seeman E.
        • et al.
        The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis.
        N Engl J Med. 2004; 350: 459-468
        • Bruyere O.
        • Collette J.
        • Rizzoli R.
        • et al.
        Relationship between 3-month changes in biochemical markers of bone remodelling and changes in bone mineral density and fracture incidence in patients treated with strontium ranelate for 3 years.
        Osteoporos Int. 2010; 21: 1031-1036
        • Quesada-Gomez J.M.
        • Muschitz C.
        • Gomez-Reino J.
        • et al.
        The effect of PTH (1–84) or strontium ranelate on bone formation markers in postmenopausal women with primary osteoporosis: results of a randomized, open-label clinical trial.
        Osteoporos Int. 2010; ([Epub ahead of print])
        • Bjarnason N.H.
        • Sarkar S.
        • Duong T.
        • et al.
        Six and twelve month change in bone turnover are related to reduction in vertebral fracture risk during 3 years of raloxifene treatment in postmenopausal osteoporosis.
        Osteoporos Int. 2001; 12: 922-930
        • Collette J.
        • Bruyere O.
        • Kaufman J.M.
        • et al.
        Vertebral anti-fracture efficacy of strontium ranelate according to pre-treatment bone turnover.
        Osteoporos Int. 2010; 21: 233-241
        • Devogelaer J.-P.
        • Boutsen Y.
        • Manicourt D.H.
        Bisphosphonate therapy for the treatment of postmenopausal osteoporosis.
        Aging Health. 2005; 1: 1-16
        • Eastell R.
        • Christiansen C.
        • Grauer A.
        • et al.
        Effects of denosumab on bone turnover markers in postmenopausal osteoporosis.
        J Bone Miner Res. 2011; 26: 530-537
        • Delmas P.D.
        • Munoz F.
        • Black D.M.
        • et al.
        Effects of yearly zoledronic acid 5 mg on bone turnover markers and relation of PINP with fracture reduction in postmenopausal women with osteoporosis.
        J Bone Miner Res. 2009; 24: 1544-1551
        • Black D.M.
        • Delmas P.D.
        • Eastell R.
        • et al.
        Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis.
        N Engl J Med. 2007; 356: 1809-1822
        • Cummings S.R.
        • San Martin J.
        • McClung M.R.
        • et al.
        Denosumab for prevention of fractures in postmenopausal women with osteoporosis.
        N Engl J Med. 2009; 361: 756-765
        • Bergmann P.
        • Body J.J.
        • Boonen S.
        • et al.
        Evidence-based guidelines for the use of biochemical markers of bone turnover in the selection and monitoring of bisphosphonate treatment in osteoporosis: a consensus document of the Belgian Bone Club.
        Int J Clin Pract. 2009; 63: 19-26
        • Landfeldt E.
        • Ström O.
        • Robbins S.
        • et al.
        Adherence to treatment of primary osteoporosis and its association to fractures – The Swedish Adherence Register Analysis (SARA).
        Osteoporos Int. 2011; ([Epub ahead of print])
        • Delmas P.D.
        • Vrijens B.
        • Eastell R.
        • et al.
        Effects of monitoring bone turnover markers on persistence with risedronate treatment of postmenopausal osteoporosis.
        J Clin Endocrinol Metab. 2007; 92: 1296-1304
        • Black D.M.
        • Schwartz A.V.
        • Ensrud K.E.
        • et al.
        Effects of continuing or stopping alendronate after 5 years of treatment: the Fracture Intervention Trial Long-term Extension (FLEX): a randomized trial.
        JAMA. 2006; 296: 2927-2938
        • Curtis J.R.
        • Westfall A.O.
        • Cheng H.
        • et al.
        Risk of hip fracture after bisphosphonate discontinuation: implications for a drug holiday.
        Osteoporos Int. 2008; 19: 1613-1620
        • Grey A.
        • Bolland M.J.
        • Wattie D.
        • et al.
        The antiresorptive effects of a single dose of zoledronate persist for two years: a randomized, placebo-controlled trial in osteopenic postmenopausal women.
        J Clin Endocrinol Metab. 2009; 94: 538-544
        • Sellmeyer D.E.
        Atypical fractures as a potential complication of long-term bisphosphonate therapy.
        JAMA. 2010; 304: 1480-1484
        • Marx R.E.
        • Cillo Jr., J.E.
        • Ulloa J.J.
        Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment.
        J Oral Maxillofac Surg. 2007; 65: 2397-2410
        • Hillier T.A.
        • Cauley J.A.
        • Rizzo J.H.
        • et al.
        The WHO absolute fracture risk models (FRAX): do clinical risk factors improve fracture prediction in older women without osteoporosis?.
        J Bone Miner Res. 2011; ([Epub ahead of print])