Skip to main content

Advertisement

Log in

Osteoporosis in chronic inflammatory disease: the role of malnutrition

  • Mini Review
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Osteoporosis is a metabolic bone disorder affecting million of people worldwide. Increased understanding of bone disease has led to a greater recognition of factors affecting bones, and consequently many secondary causes of osteoporosis were demonstrated. In this study, we aim to explore possible causes of bone loss and fractures in subjects affected by chronic inflammatory disease and to suggest new targets for intervention. In fact several studies, evaluated to perform this study, suggest that the patients with chronic inflammatory disease could be at high risk for fractures due to bone loss as consequence of malnutrition, caused by inflammation and hormonal change. Consequently, some actions could derive from the considerations of these mechanisms: a change in actual approach of chronic patients, that may include the investigation on the possible presence of osteoporosis, as well as further research on this topic to find a better therapy to prevent osteoporosis considering all the mechanisms described.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. J.T. Lin, J.M. Lane, Osteoporosis: a review. Clin. Orthop. Relat. Res. 425, 126–134 (2004)

    Article  PubMed  Google Scholar 

  2. P. Sambrook, C. Cooper, Osteoporosis. Lancet 367, 2010–2018 (2006)

    Article  PubMed  CAS  Google Scholar 

  3. S. Khosla, B. Riggs, Pathophysiology of age-related bone loss and osteoporosis. Endocrinol. Metab. Clin. N. Am. 34, 1015–1030 (2005)

    Article  CAS  Google Scholar 

  4. S. Khosla, B. Riggs, R. Robb, J. Camp, S. Achenbach, A. Oberg, P.A. Rouleau, L.J. Melton 3rd, Relationship of volumetric bone density and structural parameters at different skeletal sites to sex steroid levels in women. J. Clin. Endocrinol. Metab. 90, 5096–5103 (2005)

    Article  PubMed  CAS  Google Scholar 

  5. K. Walker, Bone recognizing and treating secondary osteoporosis. Nat. Rev. Rheumatol. 8, 480–492 (2012)

    Article  Google Scholar 

  6. V.E. MacRae, S.C. Wong, C. Farquharson, S.F. Ahmed, Cytokine actions in growth disorders associated with pediatric chronic inflammatory diseases. Int. J. Mol. Med. 18, 1011–1018 (2006)

    PubMed  CAS  Google Scholar 

  7. T. Larussa, E. Suraci, I. Nazionale, I. Leone, T. Montalcini, L. Abenavoli, M. Imeneo, A. Pujia, F. Luzza, No evidence of circulating autoantibodies against osteoprotegerin in patients with celiac disease. World J. Gastroenterol. 14(18), 1622–1627 (2012)

    Article  Google Scholar 

  8. G.J. Tack, W.H. Verbeek, M.W. Schreurs, C.J. Mulder, The spectrum of celiac disease: epidemiology, clinical aspects and treatment. Nat. Rev. Gastroenterol. Hepatol. 4, 204–213 (2010)

    Article  Google Scholar 

  9. P. Georgiadou, S. Adamopoulos, Skeletal muscle abnormalities in chronic heart failure. Curr. Heart Fail. Rep. 9, 128–132 (2012)

    Article  PubMed  Google Scholar 

  10. T. Montalcini, V. Emanuele, R. Ceravolo, G. Gorgone, G. Sesti, F. Perticone, A. Pujia, Relation of low bone mineral density and carotid atherosclerosis in postmenopausal women. Am. J. Cardiol. 94, 266–269 (2004)

    Article  PubMed  Google Scholar 

  11. D.L. Broussard, J.H. Magnus, Coronary heart disease risk and bone mineral density among U.S. women and men. J. Womens Health 17, 479–490 (2008)

    Article  Google Scholar 

  12. R. Varma, W.S. Aronow, Y. Basis, T. Singh, K. Kalapatapu, M.B. Weiss, A.L. Pucillo, C.E. Monsen, Relation of bone mineral density to frequency of coronary heart disease. Am. J. Cardiol. 101, 1103–1104 (2008)

    Article  PubMed  Google Scholar 

  13. E. Erbilen, S. Yazici, H. Ozhan, S. Bulur, S. Ordu, M. Yazici, Relationship between angiographically documented coronary artery disease and low bone mass in men. Circ. J. 7, 1095–1098 (2007)

    Article  Google Scholar 

  14. M. Gossl, U.I. Modder, E.J. Atkinson, A. Lerman, S. Khosla, Osteocalcin expression by circulating endothelial progenitor cells in patients with coronary atherosclerosis. J. Am. Coll. Cardiol. 52, 1314–1325 (2008)

    Article  PubMed  Google Scholar 

  15. R. Ohmori, Y. Momiyama, H. Taniguchi, M. Kusuhara, H. Nakamura, F. Ohsuzu, Plasma osteopontin levels are associated with the presence and extent of coronary artery disease. Atherosclerosis 170, 333–337 (2003)

    Article  PubMed  CAS  Google Scholar 

  16. L. Graat-Verboom, M.A. Spruit, B.E. van den Borne, F.W. Smeenk, E.J. Martens, R. Lunde, E.F. Wouters, Correlates of osteoporosis in chronic obstructive pulmonary disease: an underestimated systemic component. Respir. Med. 103, 1143–1151 (2009)

    Article  PubMed  Google Scholar 

  17. G. Cascini, C. Falcone, C. Greco, B. Bertucci, S. Cipullo, O. Tamburrini, Whole-body magnetic resonance imaging for detecting bone metastases: comparison with bone scintigraphy. Radiol. Med. 113, 1157–1170 (2008)

    Article  PubMed  CAS  Google Scholar 

  18. K. Martensson, D. Chrysis, L. Savendahl, Interleukin-1 beta and TNF-alpha act in synergy to inhibit longitudinal growth in fetal rat metatarsal bones. J. Bone Miner. Res. 19, 1805–1812 (2004)

    Article  PubMed  CAS  Google Scholar 

  19. V.E. MacRae, C. Farquharson, S.F. Ahmed, The restricted potential for recovery of growth plate chondrogenesis and longitudinal bone growth following exposure to pro-inflammatory cytokines. J. Endocrinol. 189, 319–328 (2006)

    Article  PubMed  CAS  Google Scholar 

  20. J.C. Tan, R. Rabkin, Suppressors of cytokine signaling in health and disease. Pediatr. Nephrol. 20, 567–575 (2005)

    Article  PubMed  Google Scholar 

  21. E. Choy, Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxf.) 5, 3–11 (2012)

    Article  Google Scholar 

  22. A. Giustina, G. Mazziotti, E. Canalis, Growth hormone, insulin-like growth factors, and the skeleton. Endocr. Rev. 29, 535–559 (2008)

    Article  PubMed  CAS  Google Scholar 

  23. S. Ferrari-Lacraz, S. Ferrari, Do RANKL inhibitors (denosumab) affect inflammation and immunity? Osteoporos. Int. 22, 435–446 (2011)

    Article  PubMed  CAS  Google Scholar 

  24. M. Chabaud, J.M. Durand, N. Buchs, F. Fossiez, G. Page, L. Frappart et al., Human interleukin-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthr. Rheum. 42, 963–970 (1999)

    Article  CAS  Google Scholar 

  25. C.K. Wong, C.Y. Ho, E.K. Li, C.W. Lam, Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus. Lupus 9, 589–593 (2000)

    Article  PubMed  CAS  Google Scholar 

  26. K. Kurasawa, K. Hirose, H. Sano, H. Endo, H. Shinkai, Y. Nawata et al., Increased interleukin-17 production in patients with systemic sclerosis. Arthr. Rheum. 43, 2455–2463 (2000)

    Article  CAS  Google Scholar 

  27. M.A. Lowes, T. Kikuchi, J. Fuentes-Duculan, I. Cardinale, L.C. Zaba, A.S. Haider et al., Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J. Invest. Dermatol. 128, 1207–1211 (2008)

    Article  PubMed  CAS  Google Scholar 

  28. A.M. Tyagi, K. Srivastava, M.N. Mansoori, R. Trivedi, N. Chattopadhyay, D. Singh, Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: a new candidate in the pathogenesis of osteoporosis. PLoS ONE 7, e44552 (2012)

    Article  PubMed  CAS  Google Scholar 

  29. G. Schett, Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur. J. Clin. Invest. 41, 1361–1366 (2011)

    Article  PubMed  CAS  Google Scholar 

  30. S. Koch, P. Nava, C. Addis, W. Kim, T.L. Denning, L. Li, C.A. Parkos, A. Nusrat, The Wnt antagonist Dkk1 regulates intestinal epithelial homeostasis and wound repair. Gastroenterology 141, 259–268 (2011)

    Article  PubMed  CAS  Google Scholar 

  31. R. Baron, G. Rawadi, Targeting the Wnt/β catenin pathway to regulate bone formation in the adult skeleton. Endocrinology 148, 2635–2643 (2007)

    Article  PubMed  CAS  Google Scholar 

  32. C.R. Plata-Salamán, Cytokines and feeding. Int. J. Obes. 25, S48–S52 (2001)

    Article  Google Scholar 

  33. A. Inui, Cancer anorexia-cachexia syndrome: are neuropeptides the key? Cancer Res. 59, 4493–4501 (1999)

    PubMed  CAS  Google Scholar 

  34. J.M. Argiles, S. Busquets, F.J. Lopez-Soriano, The pivotal role of cytokines in muscle wasting during cancer. Int. J. Biochem. Cell Biol. 37, 1609–1619 (2005)

    Article  PubMed  CAS  Google Scholar 

  35. J.M. Argilés, S. Busquets, F.J. López-Soriano, Anti-inflammatory therapies in cancer cachexia. Eur. J. Pharmacol. 1, 81–86 (2011)

    Article  Google Scholar 

  36. M.B. Reid, Y.P. Li, Tumor necrosis factor-alpha and muscle wasting: a cellular perspective. Respir. Res. 2, 269–272 (2001)

    Article  PubMed  CAS  Google Scholar 

  37. A. Laviano, M.M. Meguid, F. Rossi-Fanelli, Cancer anorexia: clinical implications, pathogenesis, and therapeutic strategies. Lancet Oncol. 4, 686–694 (2003)

    Article  PubMed  CAS  Google Scholar 

  38. A. Tournadre, P. Miossec, Interleukin-17 in inflammatory myopathies. Curr. Rheumatol. Rep. 14, 252–256 (2012)

    Article  PubMed  CAS  Google Scholar 

  39. J. von Maltzahn, N.C. Chang, C.F. Bentzinger, M.A. Rudnicki, Wnt signaling in myogenesis. Trends Cell Biol. (2012)

  40. R. Faggioni, K.R. Feingold, C. Grunfeld, Leptin regulation of the immune response and the immunodeficiency of malnutrition. FASEB J. 14, 2565–2571 (2001)

    Article  Google Scholar 

  41. V. Sanna, A. Di Giacomo, A. La Cava, R.I. Lechler, S. Fontana, S. Zappacosta, G. Matarese, Leptin surge precedes onset of autoimmune encephalomyelitis and correlates with development of pathogenic T cell responses. J Clin Invest. 111, 241–250 (2003)

    PubMed  CAS  Google Scholar 

  42. M. Otero, R. Lago, F. Lago, F.F. Casanueva, C. Dieguez, J.J. Gómez-Reino, O. Gualillo, Leptin, from fat to inflammation: old questions and new insights. FEBS Lett. 579, 295–301 (2005)

    Article  PubMed  CAS  Google Scholar 

  43. H.S. Berner, S.P. Lyngstadaas, A. Spahr, M. Monjo, L. Thommesen, C.A. Drevon, U. Syversen, J.E. Reseland, Adiponectin and its receptors are expressed in bone-forming cells. Bone 35, 842–849 (2004)

    Article  PubMed  CAS  Google Scholar 

  44. C. Roux, A. Arabi, R. Porcher, P. Garnro, Serum leptin as a determinant of bone resorption in healthy postmenopausal women. Bone 33, 837–852 (2003)

    Article  Google Scholar 

  45. J.M. Gimble, M.E. Nuttall, Bone and fat: old questions, new insights. Endocrine 23, 183–188 (2004)

    Article  PubMed  CAS  Google Scholar 

  46. G. Musso, Non-alcoholic fatty liver, adipose tissue, and the bone: a new triumvirate on the block. Endocrine (2012). doi:10.1007/s12020-012-9748-2

  47. G.S. Kim, J.S. Hong, S.W. Kim, J.M. Koh, C.S. An, J.Y. Choi, S.L. Cheng, Leptin induces apoptosis via ERK/cPLA2/cytochrome c pathway in human bone marrow stromal cells. J. Biol. Chem. 13, 21920–21929 (2003)

    Article  Google Scholar 

  48. H. Blain, A. Vuillemin, F. Guillemin, B. Hanesse, N. de Talance, B. Doucet, C. Jeandel, Serum leptin levels is a predictor of bone mineral density in postmenopausal women. J. Clin. Endocrinol. Metab. 87, 1030–1035 (2002)

    Article  PubMed  CAS  Google Scholar 

  49. A. Goulding, R.W. Taylor, Plasma leptin values in relation to bone mass and density to dynamic biochemical markers of bone resorption and formation in postmenopausal women. Calcif. Tissue Int. 63, 56–458 (1998)

    Article  Google Scholar 

  50. M. Yamauchi, T. Sugimoto, T. Yamaguchi, D. Nakaoka, M. Kanzawa, S. Yano, R. Ozuru, T. Sugishita, K. Chihara, Plasma leptin concentrations are associated with bone mineral density and presence of vertebral fractures in postmenopausal women. Clin. Endocrinol. (Oxf.) 55, 341–347 (2001)

    Article  CAS  Google Scholar 

  51. M.D. Kontogianni, U.G. Dafni, J.G. Routsias, F.N. Skopouli, Blood leptin and resistin as possible mediators of the relation between fat mass and BMD in perimenopausal women. J. Bone Miner. Res. 19, 546–551 (2004)

    Article  PubMed  CAS  Google Scholar 

  52. F. Rauch, W.F. Blum, K. Klein, B. Allolio, E. Schonau, Does leptin have an effect on bone in adult women? Calcif. Tissue Int. 63, 453–455 (1998)

    Article  PubMed  CAS  Google Scholar 

  53. M. Yılmaz, I. Keles, G. Aydın, S. Orkun, M. Bayram, F.C. Sevinc, U. Kisa, I. Yetkin, Plasma leptin concentration in postmenopausal women with osteoporosis. Endocr. Res. 31, 133–138 (2005)

    Article  Google Scholar 

  54. G. Sahin, G. Polat, S. Bagis, A. Milcan, O. Bagdatoglu, C. Erdogan, H. Camdeviren, Body composition, bone mineral density and circulating leptin levels in postmenopausal Turkish women. Rhematol. Int. 23, 87–91 (2003)

    CAS  Google Scholar 

  55. M. Shaarawy, A.F. Abassi, H. Hassan, M.E. Salem, Relationship between serum leptin concentrations and bone mineral density as well as biochemical markers of bone turnover in women with postmenopausal osteoporosis. Fertil. Steril. 79, 919–924 (2003)

    Article  PubMed  Google Scholar 

  56. P. Marie, F. Debias, M. Cohen-Solal, M.C. Vernejoul, New factors controlling bone remodeling. Joint Bone Spine 67, 150–156 (2000)

    PubMed  CAS  Google Scholar 

  57. P. Xue, P. Gao, Y. Li, The association between metabolic syndrome and bone mineral density: a meta-analysis. Endocrine (2012). doi:10.1007/s12020-012-9684-1

  58. S. Pinto, A.G. Roseberry, H. Liu, S. Diano, M. Shanabrough, X. Cai, J.M. Friedman, T.L. Horvath, Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304, 110–115 (2004)

    Article  PubMed  CAS  Google Scholar 

  59. R.E. Hubbard, M.S. O’Mahony, B.L. Calver, K.W. Woodhouse, Nutrition, inflammation, and leptin levels in aging and frailty. J. Am. Geriatr. Soc. 56, 279–284 (2008)

    Article  PubMed  Google Scholar 

  60. E. Toussirot, D. Binda, C. Gueugnon, G. Dumoulin, Adiponectin in autoimmune diseases. Curr. Med. Chem. (2012). [Epub ahead of print]

  61. K.E. Barbour, J.M. Zmuda, R. Boudreau, E.S. Strotmeyer, M.J. Horwitz, R.W. Evans, Health ABC Study et al., The effects of adiponectin and leptin on changes in bone mineral density. Osteoporos. Int. 23, 1699–1710 (2012)

    Article  PubMed  CAS  Google Scholar 

  62. K.E. Barbour, J.M. Zmuda, R. Boudreau, E.S. Strotmeyer, M.J. Horwitz, R.W. Evans et al., Adipokines and the risk of fracture in older adults. J. Bone Miner. Res. 26, 1568–1576 (2011)

    Article  PubMed  CAS  Google Scholar 

  63. E. Guillod-Maximin, A.F. Roy, C.M. Vacher, A. Aubourg, V. Bailleux, A. Lorsignol et al., Adiponectin receptors are expressed in hypothalamus and colocalized with proopiomelanocortin and neuropeptide Y in rodent arcuate neurons. J. Endocrinol. 200, 93–105 (2009)

    Article  PubMed  CAS  Google Scholar 

  64. T. Constans, Y. Bacq, J.F. Brechot, J.L. Guilmot, P. Choutet, F. Lamisse, Protein-energy malnutrition in elderly medical patients. J. Am. Geriatr. Soc. 40, 263–268 (1992)

    PubMed  CAS  Google Scholar 

  65. J. Woo, Y.T. Mak, R. Swaminathan, Nutritional status of general medical patients: influence of age and disease. J. Nutr. Biochem. 2, 274–280 (1991)

    Article  Google Scholar 

  66. R.C. Nelson, L.R. Franzi, Nutrition and aging. Med. Clin. N. Am. 73, 1531–1550 (1989)

    PubMed  CAS  Google Scholar 

  67. J.P. McWhirter, C.R. Pennington, Incidence and recognition of malnutrition in hospital. Br. Med. J. 308, 945–948 (1994)

    Article  CAS  Google Scholar 

  68. J.E. Morley, A.J. Silver, M. Fiatarone, A.D. Mooradian, Geriatric grand rounds: nutrition and the elderly. J. Am. Geriatr. Soc. 34, 823–832 (1986)

    PubMed  CAS  Google Scholar 

  69. D.H. Sullivan, G.A. Patch, R.C. Walls, D.A. Lipschitz, Impact of nutrition status on morbidity and mortality in a select population of geriatric rehabilitation patients. Am. J. Clin. Nutr. 51, 749–758 (1990)

    PubMed  CAS  Google Scholar 

  70. R.K. Chandra, The relation between immunology, nutrition and disease in elderly people. Age Ageing 19, 25–31 (1990)

    Article  Google Scholar 

  71. M.A. Fiatarone, W.J. Evans, The etiology and reversibility of muscle dysfunction in the aged. J. Gerontol. 48, 77–83 (1993)

    Article  PubMed  Google Scholar 

  72. A.N. Galanos, C.F. Pieper, J.C. Cornoni-Huntley, C.W. Bales, G.G. Fillenbaum, Nutrition and function: is there a relationship between body mass index and the functional capabilities of community-dwelling elderly? J. Am. Geriatr. Soc. 42, 368–373 (1994)

    PubMed  CAS  Google Scholar 

  73. J. Lopes, D.M. Russell, J. Whitwell, K.N. Jeejeebhoy, Skeletal muscle function in malnutrition. Am. J. Clin. Nutr. 36, 602–610 (1982)

    PubMed  CAS  Google Scholar 

  74. M.J. Ronis, K. Mercer, J.R. Chen, Effects of nutrition and alcohol consumption on bone loss. Curr. Osteoporos. Rep. 9, 53–59 (2011)

    Article  PubMed  Google Scholar 

  75. J.P. Bonjour, Calcium and phosphate: a duet of ions playing for bone health. J. Am. Coll. Nutr. 30, 438S–448S (2011)

    PubMed  CAS  Google Scholar 

  76. P. Bordelon, M.V. Ghetu, R. Langan, Recognition and management of vitamin D deficiency. Am. Fam. Physician 80, 841–846 (2009)

    PubMed  Google Scholar 

  77. S. Boonen, H.A. Bischoff-Ferrari, C. Cooper, P. Lips, O. Ljunggren, P.J. Meunier, J.Y. Reginster, Addressing the musculoskeletal components of fracture risk with calcium and vitamin D: a review of the evidence. Calcif. Tissue Int. 78, 257–270 (2006)

    Article  PubMed  CAS  Google Scholar 

  78. G. Isaia, R. Giorgino, G.B. Rini, M. Bevilacqua, D. Maugeri, S. Adami, Prevalence of hypovitaminosis D in elderly women in Italy: clinical consequences and risk factors. Osteoporos. Int. 14, 577–582 (2003)

    Article  PubMed  CAS  Google Scholar 

  79. O. Sahota, M.K. Mundey, P. San, I.M. Godber, D.J. Hosking, Vitamin D insufficiency and the blunted PTH response in established osteoporosis: the role of magnesium deficiency. Osteoporos. Int. 17, 1013–1021 (2006)

    Article  PubMed  CAS  Google Scholar 

  80. J. Aaseth, G. Boivin, O. Andersen, Osteoporosis and trace elements—an overview. J. Trace Elem. Med. Biol. 26, 149–152 (2012)

    Article  PubMed  CAS  Google Scholar 

  81. M.A. Daamen, J.M. Schols, T. Jaarsma, J.P. Hamers, Prevalence of heart failure in nursing homes: a systematic literature review. Scand. J. Caring Sci. 24, 202–208 (2010)

    Article  PubMed  Google Scholar 

  82. J.M. Chandler, S.I. Zimmerman, C.J. Girman, A.R. Martin, W. Hawkes, J.R. Hebel, P.D. Sloane, L. Holder, J. Magaziner, Low bone mineral density and risk of fracture in white female nursing home residents. J. Am. Med. Assoc. 30(284), 972–977 (2000)

    Article  Google Scholar 

  83. R. Thibault, C. Pichard, The evaluation of body composition: a useful tool for clinical practice. Ann. Nutr. Metab. 60, 6–16 (2012)

    Article  PubMed  CAS  Google Scholar 

  84. A.D. Anastasilakis, K.A. Toulis, S.A. Polyzos, C.D. Anastasilakis, P. Makras, Long-term treatment of osteoporosis: safety and efficacy appraisal of denosumab. Ther. Clin. Risk Manag. 8, 295–306 (2012)

    Article  PubMed  CAS  Google Scholar 

  85. G. Mazziotti, J. Bilezikian, E. Canalis, D. Cocchi, A. Giustina, New understanding and treatments for osteoporosis. Endocrine 41, 58–69 (2012)

    Article  PubMed  CAS  Google Scholar 

  86. C. Roggia, Y. Gao, S. Cenci, M.N. Weitzmann, G. Toraldo, G. Isaia, R. Pacifici, Upregulation of TNF-producing T cells in the bone marrow: a key mechanism by which estrogen deficiency induces bone loss in vivo. Proc. Natl Acad. Sci. U. S. A. 98, 13960–13965 (2001)

    Article  PubMed  CAS  Google Scholar 

  87. R. Kimble, S. Bain, R. Pacifici, The functional block of TNF but not of IL-6 prevents bone loss in ovariectomized mice. J. Bone Miner. Res. 12, 935–941 (1997)

    Article  PubMed  CAS  Google Scholar 

  88. K. Sinningen, E. Tsourdi, M. Rauner, T.D. Rachner, C. Hamann, L.C. Hofbauer, Skeletal and extraskeletal actions of denosumab. Endocrine 42, 52–62 (2012)

    Article  PubMed  CAS  Google Scholar 

  89. B.F. Ricciardi, J. Paul, A. Kim, L.A. Russell, J.M. Lane, Osteoporosis drug therapy strategies in the setting of disease-modifying agents for autoimmune disease. Osteoporos. Int. (2012). doi:10.1007/s00198-012-2113-8

  90. S. Wei, H. Kitaura, P. Zhou, F.P. Ross, S.L. Teitelbaum, IL-1 mediates TNF-induced osteoclastogenesis. J. Clin. Invest. 115, 282–290 (2005)

    PubMed  CAS  Google Scholar 

Download references

Conflict of interest

All authors state that they have no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiziana Montalcini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Montalcini, T., Romeo, S., Ferro, Y. et al. Osteoporosis in chronic inflammatory disease: the role of malnutrition. Endocrine 43, 59–64 (2013). https://doi.org/10.1007/s12020-012-9813-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-012-9813-x

Keywords

Navigation