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Erschienen in: Endocrine 2/2018

11.12.2017 | Original Article

Predictors of improvement in bone mineral density after celiac disease diagnosis

verfasst von: Haley M. Zylberberg, Benjamin Lebwohl, Arindam RoyChoudhury, Marcella D. Walker, Peter H. R. Green

Erschienen in: Endocrine | Ausgabe 2/2018

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Abstract

Purpose

Low bone density is frequently found in patients newly diagnosed with celiac disease (CD), and improvement is variable. This study was performed to assess changes in bone mineral density (BMD) by dual x-ray absorptiometry (DXA) at the lumbar spine, hip, and distal one-third radius as well as clinical predictors of BMD changes after the diagnosis and treatment of CD.

Methods

Adult CD patients who had serial DXA at the Celiac Disease Center at Columbia University Medical Center were included (N = 103). We assessed within-person changes in BMD with paired t-tests. Multiple regression was utilized to assess baseline clinical and laboratory predictors of BMD improvement after diagnosis and treatment.

Results

The mean age of our sample was 45.6 years (±SD 15.1) and 60% were female. After a median follow-up of 21 months, lumbar spine BMD increased by 1.7 ± 5.5% (p = 0.006) after CD diagnosis. There was a similar trend at the total hip (1.6 ± 6.3%, p = 0.06), but no change at the femoral neck or distal one-third radius. Lower baseline serum calcium predicted a greater increase in lumber spine BMD (ß = −0.0470 g/cm2, p = 0.002). At the hip, higher baseline creatinine clearance (ß = 0.005, p = 0.02) was associated with greater gains in BMD.

Conclusion

BMD increases at the lumbar spine after the diagnosis of CD and greater BMD improvement is associated with lower baseline serum calcium. This suggests that those with the lowest calcium, which is likely a surrogate for the greatest malabsorption, may have the greatest potential for improvement in skeletal health after treatment of CD.
Literatur
1.
Zurück zum Zitat D.A. Leffler, P.H. Green, A. Fasano, Extraintestinal manifestations of coeliac disease. Nat. Rev. Gastroenterol. Hepatol. 12, 561–571 (2015)CrossRefPubMed D.A. Leffler, P.H. Green, A. Fasano, Extraintestinal manifestations of coeliac disease. Nat. Rev. Gastroenterol. Hepatol. 12, 561–571 (2015)CrossRefPubMed
2.
Zurück zum Zitat G.R. Corazza, M. Di Stefano, E. Maurino, J.C. Bai, Bones in coeliac disease: diagnosis and treatment. Best Pract. Res. Clin. Gastroenterol. 19, 453–465 (2005)CrossRefPubMed G.R. Corazza, M. Di Stefano, E. Maurino, J.C. Bai, Bones in coeliac disease: diagnosis and treatment. Best Pract. Res. Clin. Gastroenterol. 19, 453–465 (2005)CrossRefPubMed
3.
Zurück zum Zitat T. Kemppainen, H. Kroger, E. Janatuinen, I. Arnala, P. Pikkarainen, J. Jurvelin, E. Alhava, M. Uusitupa, Osteoporosis in adult patients with celiac disease. Bone 24, 249–255 (1999)CrossRefPubMed T. Kemppainen, H. Kroger, E. Janatuinen, I. Arnala, P. Pikkarainen, J. Jurvelin, E. Alhava, M. Uusitupa, Osteoporosis in adult patients with celiac disease. Bone 24, 249–255 (1999)CrossRefPubMed
4.
Zurück zum Zitat A.J. Lucendo, A. García-Manzanares, Bone mineral density in adult celiac disease: an updated review. Rev. Esp. Enferm. Dig. 105, 154–162 (2013)CrossRefPubMed A.J. Lucendo, A. García-Manzanares, Bone mineral density in adult celiac disease: an updated review. Rev. Esp. Enferm. Dig. 105, 154–162 (2013)CrossRefPubMed
5.
Zurück zum Zitat D. Meyer, S. Stavropolous, B. Diamond, E. Shane, P.H. Green, Osteoporosis in a north american adult population with celiac disease. Am. J. Gastroenterol. 96, 112–129 (2001)PubMed D. Meyer, S. Stavropolous, B. Diamond, E. Shane, P.H. Green, Osteoporosis in a north american adult population with celiac disease. Am. J. Gastroenterol. 96, 112–129 (2001)PubMed
6.
Zurück zum Zitat S. Pantaleoni, M. Luchino, A. Adriani, R. Pellicano, D. Stradella, D.G. Ribaldone, N. Sapone, G.C. Isaia, M. Di Stefano, M. Astegiano, Bone mineral density at diagnosis of celiac disease and after 1 year of gluten-free diet. Sci. World J. 108, E9 (2014) S. Pantaleoni, M. Luchino, A. Adriani, R. Pellicano, D. Stradella, D.G. Ribaldone, N. Sapone, G.C. Isaia, M. Di Stefano, M. Astegiano, Bone mineral density at diagnosis of celiac disease and after 1 year of gluten-free diet. Sci. World J. 108, E9 (2014)
7.
8.
Zurück zum Zitat R. Mazure, H. Vazquez, D. Gonzalez, C. Maualen, S. Pedreira, L. Boerr, J.C. Bai, Bone mineral affection in asymptomatic adult patients with celiac disease. Am. J. Gastroenterol. 89, 2130–2134 (1994)PubMed R. Mazure, H. Vazquez, D. Gonzalez, C. Maualen, S. Pedreira, L. Boerr, J.C. Bai, Bone mineral affection in asymptomatic adult patients with celiac disease. Am. J. Gastroenterol. 89, 2130–2134 (1994)PubMed
9.
Zurück zum Zitat D. Agardh, S. Björck, C.D. Agardh, J. Lidfeldt, Celiac disease-specific tissue transglutaminase autoantibodies are associated with osteoporosis and related fractures in middle-aged women. Scand. J. Gastroenterol. 44, 571–578 (2009)CrossRefPubMed D. Agardh, S. Björck, C.D. Agardh, J. Lidfeldt, Celiac disease-specific tissue transglutaminase autoantibodies are associated with osteoporosis and related fractures in middle-aged women. Scand. J. Gastroenterol. 44, 571–578 (2009)CrossRefPubMed
10.
Zurück zum Zitat NIH consensus development panel on osteoporosis prevention, diagnosis, and therapy, March 7–29, 2000, highlights of the conference. South Med J. 94, 569–573 (2001) NIH consensus development panel on osteoporosis prevention, diagnosis, and therapy, March 7–29, 2000, highlights of the conference. South Med J. 94, 569–573 (2001)
11.
Zurück zum Zitat M. Olmos, M. Antelo, H. Vazquez, E. Smecuol, E. Maurino, J.C. Bai, Systematic review and meta-analysis of observational studies on the prevalence of fractures in coeliac disease. Dig. Liver Dis. 40, 46–53 (2008)CrossRefPubMed M. Olmos, M. Antelo, H. Vazquez, E. Smecuol, E. Maurino, J.C. Bai, Systematic review and meta-analysis of observational studies on the prevalence of fractures in coeliac disease. Dig. Liver Dis. 40, 46–53 (2008)CrossRefPubMed
12.
Zurück zum Zitat K. Heikkilä, J. Pearce, M. Mäki, K. Kaukinen, Celiac disease and bone fractures: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 100, 25–34 (2015)CrossRefPubMed K. Heikkilä, J. Pearce, M. Mäki, K. Kaukinen, Celiac disease and bone fractures: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 100, 25–34 (2015)CrossRefPubMed
13.
Zurück zum Zitat G.R. Corazza, A. Di Sario, L. Cecchetti, R.A. Jorizzo, M. Di Stefano, L. Minguzzi, G. Brusco, M. Bernardi, G. Gasbarrini, Influence of pattern of clinical presentation and of gluten-free diet on bone mass and metabolism in adult coeliac disease. Bone 18, 525–530 (1996)CrossRefPubMed G.R. Corazza, A. Di Sario, L. Cecchetti, R.A. Jorizzo, M. Di Stefano, L. Minguzzi, G. Brusco, M. Bernardi, G. Gasbarrini, Influence of pattern of clinical presentation and of gluten-free diet on bone mass and metabolism in adult coeliac disease. Bone 18, 525–530 (1996)CrossRefPubMed
15.
Zurück zum Zitat C. Sategna-Guidetti, S.B. Grosso, S. Grosso, G. Mengozzi, G. Aimo, T. Zaccaria, M. Di Stefano, G.C. Isaia, 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, 35–43 (2000)CrossRefPubMed C. Sategna-Guidetti, S.B. Grosso, S. Grosso, G. Mengozzi, G. Aimo, T. Zaccaria, M. Di Stefano, G.C. Isaia, 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, 35–43 (2000)CrossRefPubMed
16.
Zurück zum Zitat J. Szymczak, A. Bohdanowicz-Pawlak, E. Waszczuk, J. Jakubowska, Low bone mineral density in adult patients with coeliac disease. Endokrynol. Pol. 63, 270–276 (2012)PubMed J. Szymczak, A. Bohdanowicz-Pawlak, E. Waszczuk, J. Jakubowska, Low bone mineral density in adult patients with coeliac disease. Endokrynol. Pol. 63, 270–276 (2012)PubMed
17.
Zurück zum Zitat T. Larussa, E. Suraci, M. Imeneo, Normal bone mineral density associates with duodenal mucosa healing in adult patients with celiac disease on a gluten-free diet. Nutrients 9, E98 (2017)CrossRefPubMed T. Larussa, E. Suraci, M. Imeneo, Normal bone mineral density associates with duodenal mucosa healing in adult patients with celiac disease on a gluten-free diet. Nutrients 9, E98 (2017)CrossRefPubMed
18.
Zurück zum Zitat L.M. Kotze, T. Skare, A. Vinholi, L. Jurkonis, R. Nisihara, Impact of a gluten-free diet on bone mineral density in celiac patients. Rev. Esp. Enferm. Dig. 108, 84–88 (2016)PubMed L.M. Kotze, T. Skare, A. Vinholi, L. Jurkonis, R. Nisihara, Impact of a gluten-free diet on bone mineral density in celiac patients. Rev. Esp. Enferm. Dig. 108, 84–88 (2016)PubMed
19.
Zurück zum Zitat M.J. Bolland, A. Grey, D.S. Rowbotham, Outcomes of bone density measurements in coeliac disease. N. Z. Med J. 129, 40–44 (2016)PubMed M.J. Bolland, A. Grey, D.S. Rowbotham, Outcomes of bone density measurements in coeliac disease. N. Z. Med J. 129, 40–44 (2016)PubMed
20.
Zurück zum Zitat M.B. Zanchetta, V. Longobardi, F. Costa, G. Longarino, R.M. Mazure, M.L. Moreno, H. Vazquez, F. Silveira, S. Niveloni, E. Smecuol, M. de la Paz Tamprano, F. Massari, E. Sugai, A. Gonzalez, E.C. Maurino, C. Bofado, J.R. Zanchetta, J.C. Bai, Impaired bone microarchitecture improves after one year on gluten-free diet: a prospective longitudinal HRpQCT study in women with celiac disease. J. Bone Miner. Res 32, 135–142 (2017)CrossRefPubMed M.B. Zanchetta, V. Longobardi, F. Costa, G. Longarino, R.M. Mazure, M.L. Moreno, H. Vazquez, F. Silveira, S. Niveloni, E. Smecuol, M. de la Paz Tamprano, F. Massari, E. Sugai, A. Gonzalez, E.C. Maurino, C. Bofado, J.R. Zanchetta, J.C. Bai, Impaired bone microarchitecture improves after one year on gluten-free diet: a prospective longitudinal HRpQCT study in women with celiac disease. J. Bone Miner. Res 32, 135–142 (2017)CrossRefPubMed
21.
Zurück zum Zitat C. Ciacci, L. Maurelli, M. Klain, G. Savino, M. Salvatore, G. Mazzacca, M. Cirillo, Effects of dietary treatment on bone mineral density in adults with celiac disease: factors predicting response. Am. J. Gastroenterol. 92, 992–996 (1997)PubMed C. Ciacci, L. Maurelli, M. Klain, G. Savino, M. Salvatore, G. Mazzacca, M. Cirillo, Effects of dietary treatment on bone mineral density in adults with celiac disease: factors predicting response. Am. J. Gastroenterol. 92, 992–996 (1997)PubMed
22.
Zurück zum Zitat J.C. Bai, D. Gonzalez, C. Mautalen, R. Mazure, S. Pedreira, H. Vazquez, E. Smecuol, A. Siccardi, M. Cataldi, S. Niveloni, L.A. Boerr, E. Maurino, Long-term effect of gluten restriction on bone mineral density of patients with coeliac disease. Aliment. Pharmacol. Ther. 11, 157–164 (1997)CrossRefPubMed J.C. Bai, D. Gonzalez, C. Mautalen, R. Mazure, S. Pedreira, H. Vazquez, E. Smecuol, A. Siccardi, M. Cataldi, S. Niveloni, L.A. Boerr, E. Maurino, Long-term effect of gluten restriction on bone mineral density of patients with coeliac disease. Aliment. Pharmacol. Ther. 11, 157–164 (1997)CrossRefPubMed
23.
Zurück zum Zitat S. Casella, B. Zanini, F. Lanzarotto, V. Villanacci, C. Ricci, A. Lanzino, Celiac disease in elderly adults: clinical, serological, and histological characteristics and the effect of a gluten-free diet. J. Am. Geriatr. Soc. 60, 1064–1069 (2012)CrossRefPubMed S. Casella, B. Zanini, F. Lanzarotto, V. Villanacci, C. Ricci, A. Lanzino, Celiac disease in elderly adults: clinical, serological, and histological characteristics and the effect of a gluten-free diet. J. Am. Geriatr. Soc. 60, 1064–1069 (2012)CrossRefPubMed
24.
Zurück zum Zitat T. Kemppainen, H. Kroger, E. Janatuinen, I. Arnala, C. Lamberg-Allardt, M. Karkkainen, V.M. Kosma, R. Julkunen, J. Jurvelin, E. Alhava, M. Uusitupa, Bone recovery after a gluten-free diet: a 5-year follow-up study. Bone 25, 355–360 (1999)CrossRefPubMed T. Kemppainen, H. Kroger, E. Janatuinen, I. Arnala, C. Lamberg-Allardt, M. Karkkainen, V.M. Kosma, R. Julkunen, J. Jurvelin, E. Alhava, M. Uusitupa, Bone recovery after a gluten-free diet: a 5-year follow-up study. Bone 25, 355–360 (1999)CrossRefPubMed
25.
Zurück zum Zitat M.W. Davie, I. Gaywood, E. George, P.W. Jones, T. Masud, T. Price, G.D. Summers, Excess non-spine fractures in women over 50 years with celiac disease: a cross-sectional, questionnaire-based study. Osteoporos. Int 16, 1150–1155 (2005)CrossRefPubMed M.W. Davie, I. Gaywood, E. George, P.W. Jones, T. Masud, T. Price, G.D. Summers, Excess non-spine fractures in women over 50 years with celiac disease: a cross-sectional, questionnaire-based study. Osteoporos. Int 16, 1150–1155 (2005)CrossRefPubMed
26.
Zurück zum Zitat J.F. Ludvigsson, K. Michaelsson, A. Ekbom, S.M. Montgomery, Coeliac disease and the risk of fractures-a general population-based cohort study. Aliment. Pharmacol. Ther. 25, 273–285 (2007)CrossRefPubMed J.F. Ludvigsson, K. Michaelsson, A. Ekbom, S.M. Montgomery, Coeliac disease and the risk of fractures-a general population-based cohort study. Aliment. Pharmacol. Ther. 25, 273–285 (2007)CrossRefPubMed
27.
Zurück zum Zitat S.L. Bonnick, C.C. Johnston Jr., M. Kleerekoper, R. Lindsay, P. Miller, L. Sherwood, E. Siris, Importance of precision in bone density measurements. J. Clin. Densitom. 4, 105–110 (2001)CrossRefPubMed S.L. Bonnick, C.C. Johnston Jr., M. Kleerekoper, R. Lindsay, P. Miller, L. Sherwood, E. Siris, Importance of precision in bone density measurements. J. Clin. Densitom. 4, 105–110 (2001)CrossRefPubMed
28.
Zurück zum Zitat A. Vilppula, K. Kaukinen, L. Luostarinen, I. Krekela, H. Patrikainen, R. Valve, M. Luostarinen, K. Laurila, M. Maki, P. Collin, Clinical benefit of gluten-free diet in screen-detected older celiac disease patients. BMC Gastroenterol. 11, 136 (2011)CrossRefPubMedPubMedCentral A. Vilppula, K. Kaukinen, L. Luostarinen, I. Krekela, H. Patrikainen, R. Valve, M. Luostarinen, K. Laurila, M. Maki, P. Collin, Clinical benefit of gluten-free diet in screen-detected older celiac disease patients. BMC Gastroenterol. 11, 136 (2011)CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat M.B. Zanchetta, V. Longobardi, J.C. Bai, Bone and celiac disease. Curr. Osteoporos. Rep. 14, 43–48 (2016)CrossRefPubMed M.B. Zanchetta, V. Longobardi, J.C. Bai, Bone and celiac disease. Curr. Osteoporos. Rep. 14, 43–48 (2016)CrossRefPubMed
30.
31.
Zurück zum Zitat P.L. Selby, M. Davies, J.E. Adams, E.B. Mawer, Bone loss in celiac disease is related to secondary hyperparathyroidism. J. Bone Miner. Res 14, 652–657 (1999)CrossRefPubMed P.L. Selby, M. Davies, J.E. Adams, E.B. Mawer, Bone loss in celiac disease is related to secondary hyperparathyroidism. J. Bone Miner. Res 14, 652–657 (1999)CrossRefPubMed
32.
Zurück zum Zitat H. Tilg, A.R. Moschen, A. Kaser, Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57, 684–694 (2008)CrossRefPubMed H. Tilg, A.R. Moschen, A. Kaser, Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57, 684–694 (2008)CrossRefPubMed
33.
Zurück zum Zitat C.E. Fiore, P. Pennisi, G. Ferro, B. Ximenes, L. Privitelli, R.A. Mangiafico, F. Santoro, N. Parisi, T. Lombardo, Altered osteoprotegerin/RANKL ratio and low bone mineral density in celiac paients on long-term treatment with gluten-free diet. Horm. Metab. Res 38, 417–422 (2006)CrossRefPubMed C.E. Fiore, P. Pennisi, G. Ferro, B. Ximenes, L. Privitelli, R.A. Mangiafico, F. Santoro, N. Parisi, T. Lombardo, Altered osteoprotegerin/RANKL ratio and low bone mineral density in celiac paients on long-term treatment with gluten-free diet. Horm. Metab. Res 38, 417–422 (2006)CrossRefPubMed
34.
Zurück zum Zitat P.L. Riches, E. McRorie, W.D. Fraser, C. Determann, R. van’t Hof, S.H. Ralston, Osteoporosis associated with neutralizing autoantibodies against osteoprotegerin. N. Engl. J. Med 361, 1459–1465 (2009)CrossRefPubMed P.L. Riches, E. McRorie, W.D. Fraser, C. Determann, R. van’t Hof, S.H. Ralston, Osteoporosis associated with neutralizing autoantibodies against osteoprotegerin. N. Engl. J. Med 361, 1459–1465 (2009)CrossRefPubMed
35.
Zurück zum Zitat P. Brar, G.Y. Kwon, I.I. Egbuna, S. Holleran, R. Ramakrishnan, G. Bhagat, P.H. Green, Lack of correlation of degree of villous atrophy with severity of clinical presentation of coeliac disease. Dig. Liver Dis. 39, 26–32 (2007)CrossRefPubMed P. Brar, G.Y. Kwon, I.I. Egbuna, S. Holleran, R. Ramakrishnan, G. Bhagat, P.H. Green, Lack of correlation of degree of villous atrophy with severity of clinical presentation of coeliac disease. Dig. Liver Dis. 39, 26–32 (2007)CrossRefPubMed
36.
Zurück zum Zitat H. Abu Daya, B. Lebwohl, S.K. Lewis, P.H. Green, Celiac disease patients presenting with anemia have more severe disease than those presenting with diarrhea. Clin. Gastroenterol. Hepatol. 11, 1472–1477 (2013)CrossRefPubMed H. Abu Daya, B. Lebwohl, S.K. Lewis, P.H. Green, Celiac disease patients presenting with anemia have more severe disease than those presenting with diarrhea. Clin. Gastroenterol. Hepatol. 11, 1472–1477 (2013)CrossRefPubMed
37.
Zurück zum Zitat B. Lebwohl, K. Michaëlsson, P.H. Green, J.F. Ludvigsson, Persistent mucosal damage and risk of fracture in celiac disease. J. Clin. Endocrinol. Metab. 99, 609–616 (2014)CrossRefPubMedPubMedCentral B. Lebwohl, K. Michaëlsson, P.H. Green, J.F. Ludvigsson, Persistent mucosal damage and risk of fracture in celiac disease. J. Clin. Endocrinol. Metab. 99, 609–616 (2014)CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat D. Bai, P. Brar, S. Holleran, R. Ramakrishnan, P.H. Green, Effect of gender on the manifestations of celiac disease: evidence for greater malabsorption in men. Scand. J. Gastroenterol. 40, 183–187 (2005)CrossRefPubMed D. Bai, P. Brar, S. Holleran, R. Ramakrishnan, P.H. Green, Effect of gender on the manifestations of celiac disease: evidence for greater malabsorption in men. Scand. J. Gastroenterol. 40, 183–187 (2005)CrossRefPubMed
39.
Zurück zum Zitat J.S. Lindberg, S.M. Moe, Osteoporosis in end-state renal disease. Semin. Nephrol. 19, 115–122 (1999)PubMed J.S. Lindberg, S.M. Moe, Osteoporosis in end-state renal disease. Semin. Nephrol. 19, 115–122 (1999)PubMed
Metadaten
Titel
Predictors of improvement in bone mineral density after celiac disease diagnosis
verfasst von
Haley M. Zylberberg
Benjamin Lebwohl
Arindam RoyChoudhury
Marcella D. Walker
Peter H. R. Green
Publikationsdatum
11.12.2017
Verlag
Springer US
Erschienen in
Endocrine / Ausgabe 2/2018
Print ISSN: 1355-008X
Elektronische ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-017-1488-x

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