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Published in: Osteoporosis International 3/2017

01-03-2017 | Original Article

Celiac disease is associated with reduced bone mineral density and increased FRAX scores in the US National Health and Nutrition Examination Survey

Authors: E. Kamycheva, T. Goto, C. A. Camargo Jr.

Published in: Osteoporosis International | Issue 3/2017

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Abstract

Summary

We investigated the association between celiac disease (CD) and bone mass density (BMD) and risk of osteoporotic fractures in the general US population. In children and men ≥18 years, CD was associated with reduced BMD, and in men ≥40 years, CD was associated with increased risk of osteoporotic fractures.

Introduction

Celiac disease (CD) is an autoimmune condition, characterized by inflammation of the small intestine. CD has an increasing prevalence, and if unrecognized or untreated, CD can lead to complications from malabsorption and micronutrient deficiencies. We aimed to study whether CD is an independent predictor of reduced bone mineral density (BMD) and FRAX scores in the general US population.

Methods

We used data from the National Health and Nutrition Examination Survey, 2009–2010 and 2013–2014. CD was defined by positive tissue transglutaminase IgA antibody test. Multivariable models of BMD and FRAX scores were adjusted for BMI, serum 25-hydroxyvitamin D, vitamin D and calcium supplements, milk intake, serum calcium, and smoking status, when available.

Results

In children, aged 8–17 years, CD was associated with decreased Z-scores, by 0.85 for hip and 0.46 for spine (both P < 0.001). In men aged ≥ 18 years, CD was associated with 0.06 g/cm2 decrease in BMD in hip and with 0.11 g/cm2 decrease in BMD in spine (P = 0.08 and P < 0.001, respectively). In women, there were no statistically significant differences in the multiple-adjusted model. In men aged ≥ 40 years, CD predicted FRAX scores, resulting in increased scores by 2.25 % (P = 0.006) for hip fracture and by 2.43 % (P = 0.05) for major osteoporotic fracture. CD did not predict FRAX scores in women aged ≥40 years.

Conclusion

CD is independently associated with reduced BMD in children and adults aged ≥18 years and is an independent risk factor of osteoporotic fractures in men aged ≥40 years.
Literature
1.
go back to reference Ludvigsson J, Bai JC, Biagi F, Card TR, Ciacci C, Ciclitira PJ, Green PH, Hadjivassiliou M, Holdoway A, van Heel DA, Kaukinen K, Leffler DA, Leonard JN, Lundin KE, McGough N, Davidson M, Murray JA, Swift GL, Walker MM, Zingone F, Sanders DS (2014) Diagnosis and management of adult coeliac disease: guidelines from the British Society of Gastroenterology. Gut 63(8):1210–1228. doi:10.1136/gutjnl-2013-306578 CrossRefPubMedPubMedCentral Ludvigsson J, Bai JC, Biagi F, Card TR, Ciacci C, Ciclitira PJ, Green PH, Hadjivassiliou M, Holdoway A, van Heel DA, Kaukinen K, Leffler DA, Leonard JN, Lundin KE, McGough N, Davidson M, Murray JA, Swift GL, Walker MM, Zingone F, Sanders DS (2014) Diagnosis and management of adult coeliac disease: guidelines from the British Society of Gastroenterology. Gut 63(8):1210–1228. doi:10.​1136/​gutjnl-2013-306578 CrossRefPubMedPubMedCentral
2.
go back to reference Ludvigsson JF, Leffler DA, Bai JC, Biagi F, Fasano A, Green PH, Hadjivassiliou M, Kaukinen K, Kelly CP, Leonard JN, Lundin KE, Murray JA, Sanders DS, Walker MM, Zingone F, Ciacci C (2013) The Oslo definitions for coeliac disease and related terms. Gut 62:43–52. doi:10.1136/gutjnl-2011-301346 CrossRefPubMed Ludvigsson JF, Leffler DA, Bai JC, Biagi F, Fasano A, Green PH, Hadjivassiliou M, Kaukinen K, Kelly CP, Leonard JN, Lundin KE, Murray JA, Sanders DS, Walker MM, Zingone F, Ciacci C (2013) The Oslo definitions for coeliac disease and related terms. Gut 62:43–52. doi:10.​1136/​gutjnl-2011-301346 CrossRefPubMed
3.
go back to reference Mearin ML (2007) Celiac disease among children and adolescents. Curr Probl Pediatr Adolesc Health Care 37:86–105CrossRefPubMed Mearin ML (2007) Celiac disease among children and adolescents. Curr Probl Pediatr Adolesc Health Care 37:86–105CrossRefPubMed
7.
go back to reference Paganelli M, Albanese C, Borrelli O, Civitelli F, Canitano N, Viola F, Passariello R, Cucchiara S (2007) Inflammation is the main determinant of low bone mineral density in pediatric inflammatory bowel disease. Inflamm Bowel Dis 13:416–423CrossRefPubMed Paganelli M, Albanese C, Borrelli O, Civitelli F, Canitano N, Viola F, Passariello R, Cucchiara S (2007) Inflammation is the main determinant of low bone mineral density in pediatric inflammatory bowel disease. Inflamm Bowel Dis 13:416–423CrossRefPubMed
8.
go back to reference Lucendo AJ, García-Manzanares A (2013) Bone mineral density in adult coeliac disease: an updated review. Rev Esp Enferm Dig 105:154–162CrossRefPubMed Lucendo AJ, García-Manzanares A (2013) Bone mineral density in adult coeliac disease: an updated review. Rev Esp Enferm Dig 105:154–162CrossRefPubMed
9.
go back to reference Beilfuss J, Berg V, Sneve M, Jorde R, Kamycheva E (2012) Effects of a 1-year supplementation with cholecalciferol on interleukin-6, tumor necrosis factor-alpha and insulin resistance in overweight and obese subjects. Cytokine 60:870–874. doi:10.1016/j.cyto.2012.07.032 CrossRefPubMed Beilfuss J, Berg V, Sneve M, Jorde R, Kamycheva E (2012) Effects of a 1-year supplementation with cholecalciferol on interleukin-6, tumor necrosis factor-alpha and insulin resistance in overweight and obese subjects. Cytokine 60:870–874. doi:10.​1016/​j.​cyto.​2012.​07.​032 CrossRefPubMed
12.
go back to reference Mardini HE, Westgate P, Grigorian AY (2015) Racial differences in the prevalence of celiac disease in the US population: National Health and Nutritional Examination Survey (NHANES) 2009-2012. Dig Dis Sci 60:1738–1742. doi:10.1007/s10620-014-3514-7 CrossRefPubMed Mardini HE, Westgate P, Grigorian AY (2015) Racial differences in the prevalence of celiac disease in the US population: National Health and Nutritional Examination Survey (NHANES) 2009-2012. Dig Dis Sci 60:1738–1742. doi:10.​1007/​s10620-014-3514-7 CrossRefPubMed
14.
go back to reference Choung RS, Ditah IC, Nadeau AM, Rubio-Tapia A, Marietta EV, Brantner TL, Camilleri MJ, Rajkumar V, Landgren O, Everhart JE, Murray JA (2015) Trends and racial/ethnic disparities in gluten-sensitive problems in the United States: findings from the National Health and Nutrition Examination Surveys from 1988 to 2012. Am J Gastroenterol 110:455–461. doi:10.1038/ajg.2015.8 CrossRefPubMed Choung RS, Ditah IC, Nadeau AM, Rubio-Tapia A, Marietta EV, Brantner TL, Camilleri MJ, Rajkumar V, Landgren O, Everhart JE, Murray JA (2015) Trends and racial/ethnic disparities in gluten-sensitive problems in the United States: findings from the National Health and Nutrition Examination Surveys from 1988 to 2012. Am J Gastroenterol 110:455–461. doi:10.​1038/​ajg.​2015.​8 CrossRefPubMed
15.
go back to reference Calvo MS, Whiting SJ, Barton CN (2004) Vitamin D fortification in the United States and Canada: current status and data needs. Am J Clin Nutr 80(Suppl):1710S–1716SCrossRefPubMed Calvo MS, Whiting SJ, Barton CN (2004) Vitamin D fortification in the United States and Canada: current status and data needs. Am J Clin Nutr 80(Suppl):1710S–1716SCrossRefPubMed
16.
go back to reference Jansen MA, Kiefte-de Jong JC, Gaillard R, Escher JC, Hofman A, Jaddoe VW, Hooijkaas H, Moll HA (2015) Growth trajectories and bone mineral density in anti-tissue transglutaminase antibody-positive children: the Generation R Study. Clin Gastroenterol Hepatol 13:913–920. doi:10.1016/j.cgh.2014.09.032 CrossRefPubMed Jansen MA, Kiefte-de Jong JC, Gaillard R, Escher JC, Hofman A, Jaddoe VW, Hooijkaas H, Moll HA (2015) Growth trajectories and bone mineral density in anti-tissue transglutaminase antibody-positive children: the Generation R Study. Clin Gastroenterol Hepatol 13:913–920. doi:10.​1016/​j.​cgh.​2014.​09.​032 CrossRefPubMed
17.
go back to reference Margoni D, Chouliaras G, Duscas G, Voskaki I, Voutsas N, Papadopoulou A, Panayiotou J, Roma E (2012) Bone health in children with celiac disease assessed by dual x-ray absorptiometry: effect of gluten-free diet and predictive value of serum biochemical indices. J Pediatr Gastroenterol Nutr 54:680–684. doi:10.1097/MPG.0b013e31823f5fc5 CrossRefPubMed Margoni D, Chouliaras G, Duscas G, Voskaki I, Voutsas N, Papadopoulou A, Panayiotou J, Roma E (2012) Bone health in children with celiac disease assessed by dual x-ray absorptiometry: effect of gluten-free diet and predictive value of serum biochemical indices. J Pediatr Gastroenterol Nutr 54:680–684. doi:10.​1097/​MPG.​0b013e31823f5fc5​ CrossRefPubMed
18.
go back to reference Hadjivassilliou M, Rao DG, Grünewald RA, Aeschlimann DP, Sarrigiannis PG, Hoggard N, Aeschlimann P, Mooney PD, Sanders DS (2016) Neurological dysfunction in celiac disease and non-celiac gluten sensitivity. Am J Gastroenterol. doi:10.1038/ajg.2015.434 CrossRef Hadjivassilliou M, Rao DG, Grünewald RA, Aeschlimann DP, Sarrigiannis PG, Hoggard N, Aeschlimann P, Mooney PD, Sanders DS (2016) Neurological dysfunction in celiac disease and non-celiac gluten sensitivity. Am J Gastroenterol. doi:10.​1038/​ajg.​2015.​434 CrossRef
19.
go back to reference Agardh D, Björck S, Agardh CD, Lidfeldt J (2009) Coeliac disease-specific tissue transglutaminase autoantibodies are associated with osteoporosis and related fractures in middle-aged women. Scand J Gastroenterol 44:571–578. doi:10.1080/00365520902718929 CrossRefPubMed Agardh D, Björck S, Agardh CD, Lidfeldt J (2009) Coeliac disease-specific tissue transglutaminase autoantibodies are associated with osteoporosis and related fractures in middle-aged women. Scand J Gastroenterol 44:571–578. doi:10.​1080/​0036552090271892​9 CrossRefPubMed
20.
go back to reference Meyer D, Stavropolous S, Diamond B, Shane E, Green PH (2001) Osteoporosis in a north american adult population with celiac disease. Am J Gastroenterol 96:112–119PubMed Meyer D, Stavropolous S, Diamond B, Shane E, Green PH (2001) Osteoporosis in a north american adult population with celiac disease. Am J Gastroenterol 96:112–119PubMed
26.
go back to reference Heikkilä K, Heliövaara M, Impivaara O, Kröger H, Knekt P, Rissanen H, Mäki M, Kaukinen K (2015) Celiac disease autoimmunity and hip fracture risk: findings from a prospective cohort study. J Bone Miner Res 30:630–636. doi:10.1002/jbmr.2380 CrossRefPubMed Heikkilä K, Heliövaara M, Impivaara O, Kröger H, Knekt P, Rissanen H, Mäki M, Kaukinen K (2015) Celiac disease autoimmunity and hip fracture risk: findings from a prospective cohort study. J Bone Miner Res 30:630–636. doi:10.​1002/​jbmr.​2380 CrossRefPubMed
27.
go back to reference Levy MA, McKinnon T, Barker T, Dern A, Helland T, Robertson J, Cuomo J, Wood T, Dixon BM (2015) Predictors of vitamin D status in subjects that consume a vitamin D supplement. Eur J Clin Nutr 69:84–89. doi:10.1038/ejcn.2014.133 CrossRefPubMed Levy MA, McKinnon T, Barker T, Dern A, Helland T, Robertson J, Cuomo J, Wood T, Dixon BM (2015) Predictors of vitamin D status in subjects that consume a vitamin D supplement. Eur J Clin Nutr 69:84–89. doi:10.​1038/​ejcn.​2014.​133 CrossRefPubMed
29.
go back to reference Dawson-Hughes B, National Osteoporosis Foundation Guide Committee (2008) A revised clinician’s guide to the prevention and treatment of osteoporosis. J Clin Endocrinol Metab 93:2463–2465. doi:10.1210/jc.2008-0926 CrossRef Dawson-Hughes B, National Osteoporosis Foundation Guide Committee (2008) A revised clinician’s guide to the prevention and treatment of osteoporosis. J Clin Endocrinol Metab 93:2463–2465. doi:10.​1210/​jc.​2008-0926 CrossRef
32.
go back to reference Cooper C, Atkinson EJ, Jacobsen SJ, O’Fallon WM, Melton LJ 3rd (2003) Population-based study of survival after osteoporotic fractures. Am J Epidemiol 137:1001–1005CrossRef Cooper C, Atkinson EJ, Jacobsen SJ, O’Fallon WM, Melton LJ 3rd (2003) Population-based study of survival after osteoporotic fractures. Am J Epidemiol 137:1001–1005CrossRef
33.
go back to reference Sernbo I, Johnell O (1993) Consequences of a hip fracture: a prospective study over 1 year. Osteoporos Int 3:148–153CrossRefPubMed Sernbo I, Johnell O (1993) Consequences of a hip fracture: a prospective study over 1 year. Osteoporos Int 3:148–153CrossRefPubMed
35.
go back to reference Watts NB, Adler RA, Bilezikian JP, Drake MT, Eastell R, Orwoll ES, Finkelstein JS (2012) Osteoporosis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97:1802–1822. doi:10.1210/jc.2011-3045 CrossRefPubMed Watts NB, Adler RA, Bilezikian JP, Drake MT, Eastell R, Orwoll ES, Finkelstein JS (2012) Osteoporosis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97:1802–1822. doi:10.​1210/​jc.​2011-3045 CrossRefPubMed
Metadata
Title
Celiac disease is associated with reduced bone mineral density and increased FRAX scores in the US National Health and Nutrition Examination Survey
Authors
E. Kamycheva
T. Goto
C. A. Camargo Jr.
Publication date
01-03-2017
Publisher
Springer London
Published in
Osteoporosis International / Issue 3/2017
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-016-3791-4

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