Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Osteoporosis International
Published in: Osteoporosis International 6/2014

01-06-2014 | Review

Celiac disease and risk of fracture in adults—a review

Authors: A. M. Hjelle, E. Apalset, P. Mielnik, J. Bollerslev, K. E. A. Lundin, G. S. Tell

Published in: Osteoporosis International | Issue 6/2014

Login to get access

Abstract

Patients with celiac disease (CD) have low bone mineral density. Evidence of increased fracture risk in these patients is conflicting, and the indication for bone mineral density screening of all adult CD patients is debated. Our aim was to review current published data on fractures in CD. Cross-sectional cohort studies and one case study were identified by searching Medline and Embase. Although the identified studies are heterogeneous and difficult to compare, the overall findings indicate a positive association between CD and risk of fracture. Adult patients with CD should be considered for bone densitometry in order to estimate fracture risk.
Literature
1.
Dube C, Rostom A, Sy R, Cranney A, Saloojee N, Garritty C, Sampson M, Zhang L, Yazdi F, Mamaladze V, Pan I, Macneil J, Mack D, Patel D, Moher D (2005) The prevalence of celiac disease in average-risk and at-risk Western European populations: a systematic review. Gastroenterology 128(4 Suppl 1):S57–S67PubMed
2.
Lohi S, Mustalahti K, Kaukinen K, Laurila K, Collin P, Rissanen H, Lohi O, Bravi E, Gasparin M, Reunanen A, Maki M (2007) Increasing prevalence of coeliac disease over time. Aliment Pharmacol Ther 26(9):1217–1225. doi:10.​1111/​j.​1365-2036.​2007.​03502 PubMed
3.
Catassi C, Kryszak D, Bhatti B, Sturgeon C, Helzlsouer K, Clipp SL, Gelfond D, Puppa E, Sferruzza A, Fasano A (2010) Natural history of celiac disease autoimmunity in a USA cohort followed since 1974. Ann Med 42(7):530–538. doi:10.​3109/​07853890.​2010.​514285 PubMed
4.
5.
Ciacci C, Cirillo M, Sollazzo R, Savino G, Sabbatini F, Mazzacca G (1995) Gender and clinical presentation in adult celiac disease. Scand J Gastroenterol 30(11):1077–1081PubMed
6.
7.
8.
Askling J, Linet M, Gridley G, Halstensen TS, Ekstrom K, Ekbom A (2002) Cancer incidence in a population-based cohort of individuals hospitalized with celiac disease or dermatitis herpetiformis. Gastroenterology 123(5):1428–1435PubMed
9.
Corrao G, Corazza GR, Bagnardi V, Brusco G, Ciacci C, Cottone M, Sategna Guidetti C, Usai P, Cesari P, Pelli MA, Loperfido S, Volta U, Calabro A, Certo M (2001) Mortality in patients with coeliac disease and their relatives: a cohort study. Lancet 358(9279):356–361PubMed
10.
Green PH, Cellier C (2007) Celiac disease. N Engl J Med 357(17):1731–1743PubMed
11.
12.
13.
Hillier TA, Stone KL, Bauer DC, Rizzo JH, Pedula KL, Cauley JA, Ensrud KE, Hochberg MC, Cummings SR (2007) Evaluating the value of repeat bone mineral density measurement and prediction of fractures in older women: the study of osteoporotic fractures. Arch Intern Med 167(2):155–160. doi:10.​1001/​archinte.​167.​2.​155 PubMed
14.
Oyen J, Brudvik C, Gjesdal CG, Tell GS, Lie SA, Hove LM (2011) Osteoporosis as a risk factor for distal radial fractures: a case-control study. J Bone Joint Surg Am 93(4):348–356. doi:10.​2106/​JBJS.​J.​00303 PubMed
15.
Casella S, Zanini B, Lanzarotto F, Villanacci V, Ricci C, Lanzini A (2012) Celiac disease in elderly adults: clinical, serological, and histological characteristics and the effect of a gluten-free diet. J Am Geriatr Soc 60(6):1064–1069. doi:10.​1111/​j.​1532-5415.​2012.​03997.​x PubMed
16.
17.
Duerksen DR, Leslie WD (2010) Positive celiac disease serology and reduced bone mineral density in adult women. Can J Gastroenterol 24(2):103–107PubMedCentralPubMed
18.
Corazza GR, Di Sario A, Cecchetti L, Tarozzi C, Corrao G, Bernardi M, Gasbarrini G (1995) Bone mass and metabolism in patients with celiac disease. Gastroenterology 109(1):122–128PubMed
19.
20.
Szymczak J, Bohdanowicz-Pawlak A, Waszczuk E, Jakubowska J (2012) Low bone mineral density in adult patients with coeliac disease. Endokrynol Pol 63(4):270–276PubMed
21.
Wishart J, Horowitz M, Need A, Nordin BE (1990) Relationship between forearm and vertebral mineral density in postmenopausal women with primary hyperparathyroidism. Arch Intern Med 150(6):1329–1331PubMed
22.
23.
Garcia-Manzanares A, Tenias JM, Lucendo AJ (2012) Bone mineral density directly correlates with duodenal Marsh stage in newly diagnosed adult celiac patients. Scand J Gastroenterol 8–9(47):927–936. doi:10.​3109/​00365521.​2012.​688217
24.
Rodrigo L (2006) Celiac disease. World J Gastroenterol 12(41):6585–6593PubMed
25.
Sategna-Guidetti C, Grosso SB, Grosso S, Mengozzi G, Aimo G, Zaccaria T, Di Stefano M, Isaia GC (2000) The effects of 1-year gluten withdrawal on bone mass, bone metabolism and nutritional status in newly-diagnosed adult coeliac disease patients. Aliment Pharmacol Ther 14(1):35–43PubMed
26.
Kemppainen T, Kroger H, Janatuinen E, Arnala I, Lamberg-Allardt C, Karkkainen M, Kosma VM, Julkunen R, Jurvelin J, Alhava E, Uusitupa M (1999) Bone recovery after a gluten-free diet: a 5-year follow-up study. Bone 25(3):355–360PubMed
27.
Bai JC, Gonzalez D, Mautalen C, Mazure R, Pedreira S, Vazquez H, Smecuol E, Siccardi A, Cataldi M, Niveloni S, Boerr LA, Maurino E (1997) Long-term effect of gluten restriction on bone mineral density of patients with coeliac disease. Aliment Pharmacol Ther 11(1):157–164PubMed
28.
29.
Valdimarsson T, Lofman O, Toss G, Strom M (1996) Reversal of osteopenia with diet in adult coeliac disease. Gut 38(3):322–327PubMedCentralPubMed
30.
McFarlane XA, Bhalla AK, Reeves DE, Morgan LM, Robertson DA (1995) Osteoporosis in treated adult coeliac disease. Gut 36(5):710–714PubMedCentralPubMed
31.
Lucendo AJ, Garcia-Manzanares A (2013) Bone mineral density in adult coeliac disease: an updated review. Rev Esp Enferm Dig Organo Off Soc Esp Patol Dig 105(3):154–162
32.
33.
34.
Kanis JA, Borgstrom F, De Laet C, Johansson H, Johnell O, Jonsson B, Oden A, Zethraeus N, Pfleger B, Khaltaev N (2005) Assessment of fracture risk. Osteoporos Int 16(6):581–589. doi:10.​1007/​s00198-004-1780-5 PubMed
35.
Valdimarsson T, Toss G, Lofman O, Strom M (2000) Three years’ follow-up of bone density in adult coeliac disease: significance of secondary hyperparathyroidism. Scand J Gastroenterol 35(3):274–280PubMed
36.
37.
Fouda MA, Khan AA, Sultan MS, Rios LP, McAssey K, Armstrong D (2012) Evaluation and management of skeletal health in celiac disease: position statement. Can J Gastroenterol 26(11):819–829PubMedCentralPubMed
38.
39.
Delco F, El-Serag HB, Sonnenberg A (1999) Celiac sprue among US military veterans: associated disorders and clinical manifestations. Dig Dis Sci 44(5):966–972PubMed
40.
41.
Lerner A, Shapira Y, Agmon-Levin N, Pacht A, Ben-Ami Shor D, Lopez HM, Sanchez-Castanon M, Shoenfeld Y (2012) The clinical significance of 25OH-vitamin D status in celiac disease. Clin Rev Allergy Immunol 42(3):322–330. doi:10.​1007/​s12016-010-8237-8 PubMed
42.
Fornari MC, Pedreira S, Niveloni S, Gonzalez D, Diez RA, Vazquez H, Mazure R, Sugai E, Smecuol E, Boerr L, Maurino E, Bai JC (1998) 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 93(3):413–418. doi:10.​1111/​j.​1572-0241.​1998.​00413.​x PubMed
43.
Jameson S (2000) Coeliac disease, insulin-like growth factor, bone mineral density, and zinc. Scand J Gastroenterol 35(8):894–896PubMed
44.
Devine A, Rosen C, Mohan S, Baylink D, Prince RL (1998) Effects of zinc and other nutritional factors on insulin-like growth factor I and insulin-like growth factor binding proteins in postmenopausal women. Am J Clin Nutr 68(1):200–206PubMed
45.
Farthing MJ, Rees LH, Dawson AM (1983) Male gonadal function in coeliac disease: III. Pituitary regulation. Clin Endocrinol 19(6):661–671
46.
Sher KS, Jayanthi V, Probert CS, Stewart CR, Mayberry JF (1994) Infertility, obstetric and gynaecological problems in coeliac sprue. Dig Dis (Basel, Switzerland) 12(3):186–190
47.
Graat-Verboom L, Smeenk FW, van den Borne BE, Spruit MA, Donkers-van Rossum AB, Aarts RP, Wouters EF (2012) Risk factors for osteoporosis in Caucasian patients with moderate chronic obstructive pulmonary disease: a case control study. Bone 50(6):1234–1239. doi:10.​1016/​j.​bone.​2012.​02.​638 PubMed
48.
49.
Baptista ML, Koda YK, Mitsunori R, Nisihara, Ioshii SO (2005) Prevalence of celiac disease in Brazilian children and adolescents with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr 41(5):621–624PubMed
50.
51.
Garcia-Manzanares A, Lucendo AJ (2011) Nutritional and dietary aspects of celiac disease. Nutr Clin Pract Off Publ Am Soc Parenter Enter Nutr 26(2):163–173. doi:10.​1177/​0884533611399773​
52.
Taranta A, Fortunati D, Longo M, Rucci N, Iacomino E, Aliberti F, Facciuto E, Migliaccio S, Bardella MT, Dubini A, Borghi MO, Saraifoger S, Teti A, Bianchi ML (2004) Imbalance of osteoclastogenesis-regulating factors in patients with celiac disease. J Bone Miner Res 19(7):1112–1121. doi:10.​1359/​jbmr.​040319 PubMed
53.
Moreno ML, Crusius JB, Chernavsky A, Sugai E, Sambuelli A, Vazquez H, Maurino E, Pena AS, Bai JC (2005) The IL-1 gene family and bone involvement in celiac disease. Immunogenetics 57(8):618–620. doi:10.​1007/​s00251-005-0033-x PubMed
54.
55.
56.
Koh JM, Khang YH, Jung CH, Bae S, Kim DJ, Chung YE, Kim GS (2005) Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: evidence for a link between systemic inflammation and osteoporosis. Osteoporos Int 16(10):1263–1271. doi:10.​1007/​s00198-005-1840-5 PubMed
57.
Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB (2007) Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res 22(7):1088–1095. doi:10.​1359/​jbmr.​070409 PubMed
58.
Olmos M, Antelo M, Vazquez H, Smecuol E, Maurino E, Bai JC (2008) Systematic review and meta-analysis of observational studies on the prevalence of fractures in coeliac disease. Dig Liver Dis 40(1):46–53. doi:10.​1016/​j.​dld.​2007.​09.​006 PubMed
59.
60.
Fickling WE, McFarlane XA, Bhalla AK, Robertson DA (2001) The clinical impact of metabolic bone disease in coeliac disease. Postgrad Med J 77(903):33–36PubMedCentralPubMed
61.
Thomason K, West J, Logan RF, Coupland C, Holmes GK (2003) Fracture experience of patients with coeliac disease: a population based survey. Gut 52(4):518–522PubMedCentralPubMed
62.
Moreno ML, Vazquez H, Mazure R, Smecuol E, Niveloni S, Pedreira S, Sugai E, Maurino E, Gomez JC, Bai JC (2004) Stratification of bone fracture risk in patients with celiac disease. Clin Gastroenterol Hepatol 2(2):127–134PubMed
63.
Davie MW, Gaywood I, George E, Jones PW, Masud T, Price T, Summers GD (2005) Excess non-spine fractures in women over 50 years with celiac disease: a cross-sectional, questionnaire-based study. Osteoporos Int 16(9):1150–1155. doi:10.​1007/​s00198-004-1822-z PubMed
64.
Vestergaard P, Mosekilde L (2002) 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 156(1):1–10PubMed
65.
West J, Logan RF, Card TR, Smith C, Hubbard R (2003) Fracture risk in people with celiac disease: a population-based cohort study. Gastroenterology 125(2):429–436PubMed
66.
Jafri MR, Nordstrom CW, Murray JA, Van Dyke CT, Dierkhising RA, Zinsmeister AR, Melton LJ 3rd (2008) Long-term fracture risk in patients with celiac disease: a population-based study in Olmsted County, Minnesota. Dig Dis Sci 53(4):964–971. doi:10.​1007/​s10620-007-9976-0 PubMedCentralPubMed
67.
68.
Sanchez MI, Mohaidle A, Baistrocchi A, Matoso D, Vazquez H, Gonzalez A, Mazure R, Maffei E, Ferrari G, Smecuol E, Crivelli A, de Paula JA, Gomez JC, Pedreira S, Maurino E, Bai JC (2011) Risk of fracture in celiac disease: gender, dietary compliance, or both? World J Gastroenterol 17(25):3035–3042. doi:10.​3748/​wjg.​v17.​i25.​3035 PubMedCentralPubMed
69.
Vilppula A, Kaukinen K, Luostarinen L, Krekela I, Patrikainen H, Valve R, Luostarinen M, Laurila K, Maki M, Collin P (2011) Clinical benefit of gluten-free diet in screen-detected older celiac disease patients. BMC Gastroenterol 11:136. doi:10.​1186/​1471-230x-11-136 PubMedCentralPubMed
70.
71.
72.
73.
Bai D, Brar P, Holleran S, Ramakrishnan R, Green PH (2005) Effect of gender on the manifestations of celiac disease: evidence for greater malabsorption in men. Scand J Gastroenterol 40(2):183–187. doi:10.​1080/​0036552051001149​8 PubMed
74.
Hasserius R, Karlsson MK, Nilsson BE, Redlund-Johnell I, Johnell O (2002) Non-participants differ from participants as regards risk factors for vertebral deformities: a source of misinterpretation in the European Vertebral Osteoporosis Study. Acta Orthop Scand 73(4):451–454. doi:10.​1080/​00016470216326 PubMed
75.
Felsenberg D, Silman AJ, Lunt M, Armbrecht G, Ismail AA, Finn JD, Cockerill WC, Banzer D, Benevolenskaya LI, Bhalla A, Bruges Armas J, Cannata JB, Cooper C, Dequeker J, Eastell R, Felsch B, Gowin W, Havelka S, Hoszowski K, Jajic I, Janott J, Johnell O, Kanis JA, Kragl G, Lopes Vaz A, Lorenc R, Lyritis G, Masaryk P, Matthis C, Miazgowski T, Parisi G, Pols HA, Poor G, Raspe HH, Reid DM, Reisinger W, Schedit-Nave C, Stepan JJ, Todd CJ, Weber K, Woolf AD, Yershova OB, Reeve J, O'Neill TW (2002) Incidence of vertebral fracture in Europe: results from the European Prospective Osteoporosis Study (EPOS). J Bone Miner Res 17(4):716–724. doi:10.​1359/​jbmr.​2002.​17.​4.​716 PubMed
76.
Melton LJ 3rd, Lane AW, Cooper C, Eastell R, O'Fallon WM, Riggs BL (1993) Prevalence and incidence of vertebral deformities. Osteoporos Int 3(3):113–119PubMed
77.
Riggs BL, Melton LJ 3rd (1995) The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone 17(5 Suppl):505S–511SPubMed
78.
79.
80.
81.
Vilppula A, Kaukinen K, Luostarinen L, Krekela I, Patrikainen H, Valve R, Maki M, Collin P (2009) Increasing prevalence and high incidence of celiac disease in elderly people: a population-based study. BMC Gastroenterol 9:49. doi:10.​1186/​1471-230x-9-49 PubMedCentralPubMed
82.
Murray JA, Van Dyke C, Plevak MF, Dierkhising RA, Zinsmeister AR, Melton LJ 3rd (2003) Trends in the identification and clinical features of celiac disease in a North American community, 1950–2001. Clin Gastroenterol Hepatol 1(1):19–27. doi:10.​1053/​jcgh.​2003.​50004 PubMed
83.
84.
Dennison EM, Compston JE, Flahive J, Siris ES, Gehlbach SH, Adachi JD, Boonen S, Chapurlat R, Diez-Perez A, Anderson FA Jr, Hooven FH, LaCroix AZ, Lindsay R, Netelenbos JC, Pfeilschifter J, Rossini M, Roux C, Saag KG, Sambrook P, Silverman S, Watts NB, Greenspan SL, Premaor M, Cooper C, Investigators G (2012) Effect of co-morbidities on fracture risk: findings from the Global Longitudinal Study of Osteoporosis in Women (GLOW). Bone 50(6):1288–1293. doi:10.​1016/​j.​bone.​2012.​02.​639 PubMed
85.
Rios LP, Khan A, Sultan M, McAssey K, Fouda MA, Armstrong D (2013) Approach to diagnosing celiac disease in patients with low bone mineral density or fragility fractures: multidisciplinary task force report. Can Fam Phys Med Fam Can 59(10):1055–1061, e1441–1058
86.
Drummond FJ, Annis P, O'Sullivan K, Wynne F, Daly M, Shanahan F, Quane KA, Molloy MG (2003) Screening for asymptomatic celiac disease among patients referred for bone densitometry measurement. Bone 33(6):970–974PubMed
87.
Gonzalez D, Sugai E, Gomez JC, Oliveri MB, Gomez Acotto C, Vega E, Bagur A, Mazure R, Maurino E, Bai JC, Mautalen C (2002) Is it necessary to screen for celiac disease in postmenopausal osteoporotic women? Calcif Tissue Int 71(2):141–144. doi:10.​1007/​s00223-001-1027-9 PubMed
88.
Lindh E, Ljunghall S, Larsson K, Lavo B (1992) Screening for antibodies against gliadin in patients with osteoporosis. J Intern Med 231(4):403–406PubMed
89.
90.
Nuti R, Martini G, Valenti R, Giovani S, Salvadori S, Avanzati A (2001) Prevalence of undiagnosed coeliac syndrome in osteoporotic women. J Intern Med 250(4):361–366PubMed
91.
Sanders DS, Patel D, Khan FB, Westbrook RH, Webber CV, Milford-Ward A, McCloskey EV (2005) Case-finding for adult celiac disease in patients with reduced bone mineral density. Dig Dis Sci 50(3):587–592PubMed
92.
Stenson WF, Newberry R, Lorenz R, Baldus C, Civitelli R (2005) Increased prevalence of celiac disease and need for routine screening among patients with osteoporosis. Arch Intern Med 165(4):393–399. doi:10.​1001/​archinte.​165.​4.​393 PubMed
93.
Karakan T, Ozyemisci-Taskiran O, Gunendi Z, Atalay F, Tuncer C (2007) Prevalence of IgA-antiendomysial antibody in a patient cohort with idiopathic low bone mineral density. World J Gastroenterol 13(21):2978–2982PubMed
94.
Armagan O, Uz T, Tascioglu F, Colak O, Oner C, Akgun Y (2005) Serological screening for celiac disease in premenopausal women with idiopathic osteoporosis. Clin Rheumatol 24(3):239–243. doi:10.​1007/​s10067-004-1011-7 PubMed
95.
Kavuncu V, Dundar U, Ciftci IH, Evcik D, Yigit I (2009) Is there any requirement for celiac disease screening routinely in postmenopausal women with osteoporosis? Rheumatol Int 29(7):841–845. doi:10.​1007/​s00296-008-0797-z PubMed
96.
Scott EM, Gaywood I, Scott BB (2000) Guidelines for osteoporosis in coeliac disease and inflammatory bowel disease. British Society of Gastroenterology. Gut 46(Suppl 1):i1–i8PubMedCentralPubMed
97.
Muhammad R, Ahmed AM, Limdi J (2012) The predictive accuracy of pre-BMD FRAX scoring in identifying the need for treating osteoporosis in patients with coeliac disease. Am J Gastroenterol 107(Suppl):S1–S880
98.
99.
Bai JC, Fried M, Corazza GR, Schuppan D, Farthing M, Catassi C, Greco L, Cohen H, Ciacci C, Eliakim R, Fasano A, Gonzalez A, Krabshuis JH, LeMair A (2013) World Gastroenterology Organisation Global Guidelines on Celiac Disease. J Clin Gastroenterol 47(2):121–126. doi:10.​1097/​MCG.​0b013e31827a6f83​ PubMed
100.
101.
102.
Metadata
Title
Celiac disease and risk of fracture in adults—a review
Authors
A. M. Hjelle
E. Apalset
P. Mielnik
J. Bollerslev
K. E. A. Lundin
G. S. Tell
Publication date
01-06-2014
Publisher
Springer London
Published in
Osteoporosis International / Issue 6/2014
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-014-2683-8

Other articles of this Issue 6/2014

Osteoporosis International 6/2014 Go to the issue

Original Article

Incident long-term warfarin use and risk of osteoporotic fractures: propensity-score matched cohort of elders with new onset atrial fibrillation

Original Article

Biochemical markers of bone turnover in diabetes patients—a meta-analysis, and a methodological study on the effects of glucose on bone markers

Letter

Comment on Cassell and Clapperton: A decreasing trend in fall-related hip fracture incidence in Victoria, Australia

Letter

The decreasing trend in hip fractures: response to Stevens & Rudd

Original Article

Effects of PTH(1–84) therapy on muscle function and quality of life in hypoparathyroidism: results from a randomized controlled trial

Original Article

TBS result is not affected by lumbar spine osteoarthritis