Bone mass and mineral metabolism alterations in adult celiac disease: Pathophysiology and clinical approach

Nutrients

Volumn 5, Issue 11, 2013, Pages 4786-4799

  Di Stefano, Michele ^a   Mengoli, Caterina ^a   Bergonzi, Manuela ^a   Corazza, Gino Roberto ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

Bone densitometry; Celiac disease; Gluten free diet; Osteoporosis

Indexed keywords

CALCIUM; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TUMOR NECROSIS FACTOR ALPHA; VITAMIN D;

ALCOHOL ABSTINENCE; BONE DENSITOMETRY; BONE DENSITY; BONE INJURY; BONE MASS; CALCIUM ABSORPTION; CALCIUM INTAKE; CAUSAL ATTRIBUTION; CELIAC DISEASE; ENTERITIS; FRACTURE; GLUTEN FREE DIET; HEALTH CARE COST; HUMAN; LIFESTYLE MODIFICATION; MALABSORPTION; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PATHOGENESIS; PHYSICAL ACTIVITY; PREVALENCE; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SMOKING CESSATION; SPINE FRACTURE; TREATMENT DURATION; TREATMENT INDICATION; TREATMENT RESPONSE; VITAMIN SUPPLEMENTATION;

ADULT; BONE AND BONES; BONE DENSITY; CALCIUM, DIETARY; CELIAC DISEASE; DIET, GLUTEN-FREE; FRACTURES, BONE; HUMANS; OSTEOPOROSIS; OSTEOPOROSIS, POSTMENOPAUSAL;

EID: 84888167583     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu5114786     Document Type: Review

References (81)

1. Consensus development conference: Prophylaxis and treatment of osteoporosis. Osteoporos. Int. 1991, 1, 114-117.
2. WHO Scientific Group on the Assessment of Osteoporosis at Primary Health Care Levels. Summary Meeting Report 2004;World Health Organization: Brussels, Belgium, 2007;pp. 1-17.
3. Corazza, G.R.;Di Sario, A.;Cecchetti, A.;Jorizzo, R.A.;Di Stefano, M.;Minguzzi, L.;Brusco, G.;Bernardi, M.;Gasbarrini, G. Influence of pattern of clinical presentation and gluten-free diet on bone mass and metabolism in adult coeliac disease. Bone 1996, 18, 525-530.
4. Mazure, R.;Vazquez, H.;Gonzalez, D.;Mautalen, C.;Pedreira, S.;Boerr, L.;Bai, J.C. Bone mineral affectation in asymptomatic adult patients with celiac disease. Am. J. Gastroenterol. 1994, 89, 2130-2134.
5. Corazza, G.R.;di Sario, A.;Cecchetti, A.;Tarozzi, C.;Corrao, G.;Bernardi, M.;Gasbarrini, G. Bone mass and metabolism in patients with celiac disease. Gastroenterology 1995, 109, 122-128.
6. McFarlane, X.A.;Bhalla, A.K.;Robertson, D.A.F. Effect of gluten free diet on osteopenia in adults with newly diagnosed celiac disease. Gut 1996, 39, 180-184.
7. Keaveny, A.P.;Freaney, R.;McKenna, M.J.;Masterson, J.;O'Donoghue, D.P. Bone remodeling indices and secondary hyperparathyroidism in celiac disease. Am. J. Gastroenterol. 1996, 91, 1226-1231.
8. Valdimarsson, T.;Löfman, O.;Toss, G.;Ström, M. Reversal of osteopenia with diet in adult coeliac disease. Gut 1996, 38, 322-327.
9. Mustalahti, K.;Collin, P.;Sievänen, H.;Salmi, J.;Mäki, M. Osteopenia in patients with clinically silent coeliac disease warrants screening. Lancet 1999, 354, 744-745.
10. Duerksen, D.R.;Leslie, W.D. Positive celiac disease serology and reduced bone mineral density in adult women. Can. J. Gastroenterol. 2010, 24, 103-107.
11. Stenson, W.F.;Newberry, R.;Lorenz, R.;Baldus, C.;Civitelli, R. Increased prevalence of celiac disease and need for routine screening among patients with osteoporosis. Arch. Intern. Med. 2005, 165, 393-399.
12. Armagan, O.;Uz, T.;Tascioglu, F.;Colak, O.;Oner, C.;Akgun, Y. Serological screening for celiac disease in premenopausal women with idiopathic osteoporosis. Clin. Rheumatol. 2005, 24, 239-243.
13. Drummond, F.J.;Annis, P.;O'Sullivan, K.;Wynne, F.;Daly, M.;Shanahan, F.;Quane, K.A.;Molloy, M.G. Screening for asymptomatic celiac disease among patients referred for bone densitometry measurement. Bone 2003, 33, 970-974.
14. Mather, K.J.;Meddings, J.B.;Beck, P.L.;Scott, R.B.;Hanley, D.A. Prevalence of IgA-antiendomysial antibody in asymptomatic low bone mineral density. Am. J. Gastroenterol. 2001, 96, 120-125.
15. Karakan, T.;Ozyemisci-Taskiran, O.;Gunendi, Z.;Atalay, F.;Tuncer, C. Prevalence of IgA-antiendomysial antibody in a patient cohort with idiopathic low bone mineral density. World J. Gastroenterol. 2007, 21, 2978-2982.
16. Molteni, N.;Bardella, M.T.;Vezzoli, G.;Pozzoli, E.;Bianchi, P. Intestinal calcium absorption as shown by stable strontium test in celiac disease before and after gluten-free diet. Am. J. Gastroenterol. 1995, 90, 2025-2028.
17. Pazianas, M.;Butcher, G.P.;Subhani, J.M.;Finch, P.J.;Ang, L.;Collins, C.;Heaney, R.P.;Zaidi, M.;Maxwell, J.D. Calcium absorption and bone mineral density in celiacs after long term treatment with gluten-free diet and adequate calcium intake. Osteoporos. Int. 2005, 16, 56-63.
18. Kinsey, L.;Burden, S.T.;Bannermann, E. A dietary survey to determine if patients with celiac disease are meeting current healthy eating guidelines and how their diet compares to that of the british general population. Eur. J. Clin. Nutr. 2008, 62, 1333-1342.
19. Plotkin, G.R.;Isselbacher, K.J. Secondary disaccharidase deficiency in adult celiac disease (Nontropical Sprue) and other malabsorption states. N. Engl. J. Med. 1964, 271, 1033-1037.
20. Valdimarsson, T.;Toss, G.;Löfman, O.;Ström, M. Three years' follow-up of bone density in adult coeliac disease: Significance of secondary hyperparathyroidism. Scand. J. Gastroenterol. 2000, 35, 274-280.
21. Corazza, G.R.;di Stefano, M.;Maurino, E.;Bai, J.C. Bones in celiac disease: Diagnosis and treatment. Best Pract. Res. Clin. Gastroenterol. 2005, 19, 453-465.
22. Staun, M.;Jarnum, S. Measurement of the 10,000-molecular weight calcium-binding protein in small-intestinal biopsy specimens from patients with malabsorption syndromes. Scand. J. Gastroenterol. 1988, 23, 827-832.
23. Colston, K.W.;Mackay, A.G.;Finlayson, C.;Wu, J.C.;Maxwell, J.D. Localisation of Vitamin D receptor in normal human duodenum and in patients with coeliac disease. Gut 1994, 35, 1219-1225.
24. Valdimarsson, T.;Arnqvist, H.J.;Toss, G.;Järnerot, G.;Nyström, F.;Ström, M. Low circulating insulin-like growth factor i in coeliac disease and its relation to bone mineral density. Scand. J. Gastroenterol. 1999, 34, 904-908.
25. Jameson, S. Coeliac disease, insulin-like growth factor, bone mineral density, and zinc. Scand. J. Gastroenterol. 2000, 35, 894-896.
26. Kontakou, M.;Przemioslo, R.T.;Sturgess, R.P.;Limb, A.G.;Ciclitira, P.J. Expression of tumour necrosis factor-alpha, interleukin-6, and interleukin-2 mRNA in the jejunum of patients with coeliac disease. Scand. J. Gastroenterol. 1995, 30, 456-463.
27. Fornari, M.C.;Pedreira, S.;Niveloni, S.;González, D.;Diez, R.A.;Vázquez, H.;Mazure, R.;Sugai, E.;Smecuol, E.;Boerr, L.;et al. Pre-and post-treatment serum levels of cytokines IL-1beta, IL-6, and IL-1 receptor antagonist in celiac disease. Are they related to the associated osteopenia? Am. J. Gastroenterol. 1998, 93, 413-418.
28. Wei, S.;Kitaura, H.;Zhou, P.;Ross, F.P.;Teitelbaum, S.L. IL-1 mediates TNF-induced osteoclastogenesis. J. Clin. Investig. 2005, 115, 282-290.
29. Raisz, L.G. Local and systemic factors in the pathogenesis of osteoporosis. N. Engl. J. Med. 1988, 318, 818-828.
30. Di Stefano, M.;Sciarra, G.;Jorizzo, R.A.;Grillo, R.L.;Cecchetti, L.;Speziale, D.;Pichini, L.;Gasbarrini, G.;Corazza, G.R. Local and gonadal factors in the pathogenesis of coeliac bone loss. Ital. J. Gastroenterol. 1997, 29, 31.
31. Taranta, A.;Fortunati, D.;Longo, M.;Rucci, N.;Iacomino, E.;Aliberti, F.;Facciuto, E.;Migliaccio, S.;Bardella, M.T.;Dubini, A. Imbalance of Osteoclastogenesis-regulating Factors in Patients with Celiac Disease. J. Bone Miner. Res. 2004, 19, 1112-1121.
32. Horwood, N.J.;Elliott, J.;Martin, T.J.;Gillespie, M.T. IL-12 alone and in synergy with IL-18 inhibits osteoclast formation in vitro. J. Immunol. 2001, 166, 4915-4921.
33. Yamada, N.;Niwa, S.;Tsujimura, T.;Iwasaki, T.;Sugihara, A.;Futani, H.;Hayashi, S.;Okamura H.;Akedo, H.;Terada, N. Interleukin-18 and interleukin-12 synergistically inhibit osteoclastic bone-resorbing activity. Bone 2002, 6, 901-908.
34. Khosla, S. Minireview: The OPG/RANKL/RANK system. Endocrinology 2001, 142, 5050-5055.
35. Fiore, C.E.;Pennisi, P.;Ferro, G.;Ximenes, B.;Privitelli, L.;Mangiafico, R.A.;Santoro, F.;Parisi, N.;Lombardo, T. Altered osteoprotegerin/RANKL ratio and low bone mineral density in celiac patients on long-term treatment with gluten-free diet. Horm. Metab. Res. 2006, 38, 417-422.
36. Riches, P.L.;McRorie, E.;Fraser, W.D.;Determann, C.;van't Hof, R.;Ralston, S.H. Osteoporosis associated with neutralizing autoantibodies against osteoprotegerin. N. Engl. J. Med. 2009, 361, 1459-1465.
37. Larussa, T.;Suraci, E.;Nazionale, I.;Leone, I.;Montalcini, T.;Abenavoli, L.;Imeneo, M.;Pujia, A.;Luzza, F. No evidence of circulating autoantibodies against osteoprotegerin in patients with celiac disease. World J. Gastroenterol. 2012, 18, 1622-1627.
38. Ozgör, B.;Selimoǧlu, M.A. Coeliac disease and reproductive disorders. Scand. J. Gastroenterol. 2010, 45, 395-402.
39. Green, J.R.;Goble, H.L.;Edwards, C.R.;Dawson, A.M. Reversible insensitivity to androgens in men with untreated gluten enteropathy. Lancet 1977, 1, 280-282.
40. Farthing, M.J.;Rees, L.H.;Dawson, A.M. Male gonadal function in coeliac disease: III. Pituitary regulation. Clin. Endocrinol. 1983, 19, 661-671.
41. Stazi, A.V.;Trecca, A.;Trinti, B. Osteoporosis in celiac disease and in endocrine and reproductive disorders. World J. Gastroenterol. 2008, 14, 498-505.
42. Di Sabatino, A.;Corazza, G.R. Coeliac disease. Lancet 2009, 373, 1480-1493.
43. Mosekilde, L.;Eriksen, E.F.;Charles, P. Effects of thyroid hormones on bone and mineral metabolism. Endocrinol. Metab. Clin. 1990, 19, 35-63.
44. Hofbauer, L.C.;Brueck, C.C.;Singh, S.K.;Dobnig, H. Osteoporosis in patients with diabetes mellitus. J. Bone Miner. Res. 2007, 22, 1317-1328.
45. Mora, S.;Barera, G.;Beccio, S.;Menni, L.;Proverbio, M.C.;Bianchi, C.;Chiumello, G. A prospective, longitudinal study of the long-term effect of treatment on bone density in children with celiac disease. J. Pediatr. 2001, 139, 516-521.
46. Mora, S.;Barera, G.;Ricotti, A.;Weber, G.;Bianchi, C.;Chiumello, G. Reversal of low bone density with a gluten-free diet in children and adolescents with celiac disease. Am. J. Clin. Nutr. 1998, 67, 477-481.
47. Bodé, S.;Hassager, C.;Gudmand-Høyer, E.;Christiansen, C. Body composition and calcium metabolism in adult treated coeliac disease. Gut 1991, 32, 1342-1345.
48. Valdimarsson, T.;Toss, G.;Ross, I.;Löfman, O.;Ström, M. Bone mineral density in coeliac disease. Scand. J. Gastroenterol. 1994, 29, 457-461.
49. Walters, J.R.;Banks, L.M.;Butcher, G.P.;Fowler, C.R. Detection of low bone mineral density by dual energy x-ray absorptiometry in unsuspected suboptimally treated coeliac disease. Gut 1995, 37, 220-224.
50. McFarlane, X.A.;Bhalla, A.K.;Reeves, D.E.;Morgan, L.M.;Robertson, D.A. Osteoporosis in treated adult coeliac disease. Gut 1995, 36, 710-714.
51. Ferretti, J.;Mazure, R.;Tanoue, P.;Marino, A.;Cointry, G.;Vazquez, H.;Niveloni, S.;Pedreira, S.;Mauriño, E.;Zanchetta, J.;et al. Analysis of the structure and strength of bones in celiac disease patients. Am. J. Gastroenterol. 2003, 98, 382-390.
52. González, D.;Mazure, R.;Mautalen, C.;Vazquez, H.;Bai, J. Body composition and bone mineral density in untreated and treated patients with celiac disease. Bone 1995, 16, 231-234.
53. Kemppainen, T.;Kröger, H.;Janatuinen, E.;Arnala, I.;Lamberg-Allardt, C.;Kärkkäinen, M.;Kosma, V.M.;Julkunen, R.;Jurvelin, J.;Alhava, E.;et al. Bone recovery after a gluten-free diet: A 5-year follow-up study. Bone 1999, 25, 355-360.
54. Corazza, G.R.;di Stefano, M.;Jorizzo, R.A.;Cecchetti, L.;Minguzzi, L.;Gasbarrini, G. Propeptide of Type I procollagen is predictive of posttreatment bone mass gain in adult celiac disease. Gastroenterology 1997, 113, 67-71.
55. Bai, J.C.;Gonzalez, D.;Mautalen, C.;Mazure, R.;Pedreira, S.;Vazquez, H.;Smecuol, E.;Siccardi, A.;Cataldi, M.;Niveloni, S.;et al. Long-term effect of gluten restriction on bone mineral density of patients with coeliac disease. Aliment. Pharm. Ther. 1997, 11, 157-164.
56. Pistorius, L.R.;Sweidan, W.H.;Purdie, D.W.;Steel, S.A.;Howey, S.;Bennett, J.R.;Sutton, D.R. Coeliac disease and bone mineral density in adult female patients. Gut 1995, 37, 639-642.
57. Kemppainen, T.;Kröger, H.;, Janatuinen, E.;Arnala, I.;Kosma, V.M.;Pikkarainen, P.;Julkunen, R.;Jurvelin, J.;Alhava, E.;Uusitupa, M. Osteoporosis in adult patients with celiac disease. Bone 1999, 24, 249-255.
58. Selby, P.L.;Davies, M.;Adams, J.E.;Mawer, E.B. Bone loss in celiac disease is related to secondary hyperparathyroidism. J. Bone Miner. Res. 1999, 14, 652-657.
59. Lemieux, B.;Boivin, M.;Brossard, J.H.;Lepage, R.;Picard, D.;Rousseau, L.;D'amour, P. Normal parathyroid function with decreased bone mineral density in treated celiac disease. Can. J. Gastroenterol. 2001, 15, 302-307.
60. Christensen, M.S.;Nielsen, H.E.;Torring, S. Hypercalcemia and parathyroid function after renal transplantation. Acta Med. Scand. 1977, 201, 35-39.
61. Liberman, U.A.;Weiss, S.R.;Bröll, J.;Minne, H.W.;Quan, H.;Bell, N.H.;Rodriguez-Portales, J.;Downs, R.W., Jr.;Dequeker, J.;Favus, M. Effect of oral alendronate on bone mineral density and the incidence of fractures in postmenopausal osteoporosis. N. Engl. J. Med. 1995, 333, 1437-1443.
62. Di Stefano, M.;Mengoli, C.;Tomarchio, O.;Bergonzi, M.;Pagani, E.;de Amici, M.;Ilardo, D.;Vattiato, C.;Biagi, F.;Zanaboni, A.;et al. Increased Osteoprotegerin and Decreased COOHTerminal Propeptide of Type I Collagen Select Celiac Disease Patients on Long Term Gluten Free Diet with Persisting Low Bone Mass. In Proceedings of UEGW (21st United European Gastroenterology Week), Belin, Germany, 12-16 October 2013.
63. Sánchez, M.I.;Mohaidle, A.;Baistrocchi, A.;Matoso, D.;Vázquez, H.;González, A.;Mazure, R.;Maffei, E.;Ferrari, G.;Smecuol, E.;et al. Risk of fracture in celiac disease: Gender, dietary compliance, or both? World J. Gastroenterol. 2011, 17, 3035-3042.
64. Bianchi, M.L.;Bardella, M.T. Bone in celiac disease. Osteoporos. Int. 2008, 19, 1705-1716.
65. West, J.;Logan, R.F.;Card, T.R.;Smith, C.;Hubbard, R. Fracture risk in people with celiac disease: A population-based cohort study. Gastroenterology 2003, 125, 429-436.
66. Jafri, M.R.;Nordstrom, C.W.;Murray, J.A.;van Dyke, C.T.;Dierkhising, R.A.;Zinsmeister, A.R.;Melton, L.J., III. Long-term fracture risk in patients with celiac disease: A population-based study in Olmsted County, Minnesota. Dig. Dis. Sci. 2008, 53, 964-971.
67. Ludvigsson, J.F.;Michaelsson, K.;Ekbom, A.;Montgomery, S.M. Coeliac disease and the risk of fractures-A general population-based cohort study. Aliment. Pharm. Ther. 2007, 25, 273-285.
68. Vasquez, H.;Mazure, R.;Gonzalez, D.;Flores, D.;Pedreira, S.;Niveloni, S.;Smecuol, E.;Mauriño, E.;Bai, J.C. Risk of fractures in celiac disease patients: A cross-sectional, case-control study. Am. J. Gastroenterol. 2000, 95, 183-189.
69. Fickling, W.E.;McFarlane, X.A.;Bhalla, A.K.;Robertson, D.A. The clinical impact of metabolic bone disease in coeliac disease. Postgrad. Med. J. 2001, 77, 33-36.
70. Davie M.W.;Gaywood, I.;George, E.;Jones, P.W.;Masud, T.;Price, T.;Summers, G.D. Excess non-spine fractures in women over 50 years with celiac disease: A cross-sectional, questionnaire-based study. Osteoporos. Int. 2005, 16, 1150-1155.
71. Moreno, M.L.;Vazquez, H.;Mazure, R.;Smecuol, E.;Niveloni, S.;Pedreira, S.;Sugai, E.;Mauriño, E.;Gomez, J.C.;Bai, J.C. Stratification of bone fracture risk in patients with celiac disease. Clin. Gastroenterol. Hepatol. 2004, 2, 127-134.
72. Olmos, M.;Antelo, M.;Vazquez, H.;Smecuol, E.;Mauriño, E.;Bai, J.C. Systematic review and meta-analysis of observational studies on the prevalence of fractures in coeliac disease. Dig. Liver Dis. 2008, 40, 46-53.
73. Vestergaard, P.;Mosekilde, L. Fracture risk in patients with celiac disease, crohn's disease, and ulcerative colitis: A nationwide follow-up study of 16,416 patients in denmark. Am. J. Epidemiol. 2002, 156, 1-10.
74. Glüer, C.C. Quantitative ultrasound techniques for the assessment of osteoporosis: Expert agreement on current status. The international quantitative ultrasound consensus group. J. Bone Miner. Res. 1997, 12, 1280-1288.
75. Njeh, C.F.;Boivin, C.M.;Langton, C.M. The role of ultrasound in the assessment of oeteoporosis: A review. Osteoporos. Int. 1997, 7, 7-22.
76. Scott, E.M.;Gaywood, I.;Scott, B.B. Guidelines for osteoporosis in coeliac disease and inflammatory bowel disease. Gut 2000, 46, I1-I8.
77. Thomason, K.;West, J.;Logan, R.F.;Coupland, C.;Holmes, G.K. Fracture experience of patients with coeliac disease: A population based survey. Gut 2003, 52, 518-522.
78. Compston, J. Is fracture risk increased in patients with coeliac disease? Gut 2003, 52, 459-460.
79. Lewis, N.R.;Scott, B.B. Should patients with coeliac disease have their bone mineral density measured? Eur. J. Gastroenterol. Hepatol. 2005, 17, 1065-1070.
80. American Gastroenterological Association. American gastroenterological association medical position statement: Guidelines on osteoporosis in gastrointestinal diseases. Gastroenterology 2003, 124, 791-794.
81. Fouda, M.A.;Khan, A.A.;Sultan, M.S.;Rios, L.P.;McAssey, K.;Armstrong, D. Evaluation and management of skeletal health in celiac disease: Position statement. Can. J. Gastroenterol. 2012, 26, 819-829.