Evaluation and Management of Skeletal Health in Celiac Disease: Position Statement
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OBJECTIVE: To review the evaluation and management of skeletal health in patients with celiac disease (CD), and to make recommendations on screening, diagnosis, treatment and follow-up of low bone mineral density (BMD) in CD patients. METHODS: A multidisciplinary team developed clinically relevant questions for review. An electronic search of the literature was conducted using the MEDLINE and EMBASE databases from 1996 to 2010. All original studies, reviews and guidelines, both pediatric and adult, were included. A document summarizing the results of the review and proposed recommendations was prepared and underwent multiple revisions until consensus was reached. RESULTS: At diagnosis, approximately one-third of adult CD patients have osteoporosis, one-third have osteopenia and one-third have normal BMD. Children with CD have low bone mass at diagnosis. Adult and pediatric CD patients are at increased risk of fractures. DISCUSSION: For adults, serum calcium, albumin, 25(OH) vitamin D 3, parathyroid hormone and 24 h urine calcium testing should be performed at diagnosis; patients with ‘classic’ CD and those at risk for osteoporosis should undergo a dual x-ray absorptiometry scan. An abnormal baseline dual x-ray absorptiometry scan should be repeated one to two years after initiation of a gluten-free diet (GFD). For children, BMD should be assessed one year after diagnosis if GFD adherence is not strict. A GFD is the most important treatment for bone loss. Supplemental antiresorptives may be justified in those who remain at high fracture risk (eg, postmenopausal women, older men) after implementation of a GFD. CONCLUSION: Current evidence does not support the screening of all CD patients for low BMD at diagnosis. Follow-up BMD assessment should be performed one to two years after initiation of a GFD.
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A reduced bone mineral density (BMD) may be present at coeliac disease diagnosis in children and adolescents.
“A reduced bone mineral density (BMD) may be present at CD diagnosis in children and adolescents (29, 32).”
From ESPGHAN Position Paper on Management and Follow-up of Children and Adolescents With Celiac Disease. (2022) · cites this paper as [32]
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A systematic review of intervention thresholds based on FRAX
The Advisory Board of the National Osteoporosis Guideline Group, Kanis, J. А., Harvey, N. C., Cooper, C. C., Johansson, H., Odén, A., & McCloskey, E. V. (2016) · Archives of Osteoporosis · doi:10.1007/s11657-016-0278-z · Cited by 421 · see citing works
Ebeling, P. R., Nguyen, H. H., Aleksova, J., Vincent, A. J., Wong, P., & Milat, F. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab028 · Cited by 354 · see citing works
Guandalini, S., & Assiri, A. A. (2014) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2013.3858 · Cited by 253 · see citing works
Practical insights into gluten-free diets
See, J. A., Kaukinen, K., Makharia, G. K., Gibson, P. R., & Murray, J. A. (2015) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2015.156 · Cited by 180 · see citing works
ESPGHAN Position Paper on Management and Follow-up of Children and Adolescents With Celiac Disease.
Mearin, M. L., Agardh, D., Antunes, H., Al‐toma, A., Auricchio, R., Castillejo, G., Catassi, C., Ciacci, C., Discepolo, V., Dolinsek, J., et al. (2022) · Journal of pediatric gastroenterology and nutrition · doi:10.1097/mpg.0000000000003540 · Cited by 186 · see citing works
The gluten‐free diet and its current application in coeliac disease and dermatitis herpetiformis
Ciacci, C., Ciclitira, P. J., Hadjivassiliou, M., Kaukinen, K., Ludvigsson, J. F., McGough, N., Sanders, D. S., Woodward, J. M., Leonard, J. N., & Swift, G. L. (2014) · United European Gastroenterology Journal · doi:10.1177/2050640614559263 · Cited by 115 · see citing works
Zanchetta, M. B., Longobardi, V., & Bai, J. C. (2016) · Current Osteoporosis Reports · doi:10.1007/s11914-016-0304-5 · Cited by 87 · see citing works
Osteoporosis in Premenopausal Women: A Clinical Narrative Review by the ECTS and the IOF
Pepe, J., Body, J., Hadji, P., McCloskey, E. V., Meier, C., Obermayer-Pietsch, B. M., Palermo, A., Tsourdi, E. A., Zillikens, M. C., Langdahl, B. L., et al. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa306 · Cited by 78 · see citing works
Stefano, M. D., Mengoli, C., Bergonzi, M., & Corazza, G. R. (2013) · Nutrients · doi:10.3390/nu5114786 · Cited by 65 · see citing works
Review article: Systemic consequences of coeliac disease
Laurikka, P., Kivelä, L., Kurppa, K., & Kaukinen, K. (2022) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.16912 · Cited by 69 · see citing works
Evidence-Informed Expert Recommendations for the Management of Celiac Disease in Children
Snyder, J., Butzner, J. D., DeFelice, A. R., Fasano, A., Guandalini, S., Liu, E., & Newton, K. P. (2016) · Pediatrics · doi:10.1542/peds.2015-3147 · Cited by 70 · see citing works
Review article: Follow‐up of coeliac disease
Tye–Din, J. A. (2022) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.16847 · Cited by 58 · see citing works
Zingone, F., Maimaris, S., Auricchio, R., Caio, G., Carroccio, A., Elli, L., Galliani, E., Montagnani, M., Valiante, F., & Biagi, F. (2022) · Digestive and Liver Disease · doi:10.1016/j.dld.2022.06.023 · Cited by 44 · see citing works
Update on Bone Health in Pediatric Chronic Disease
Williams, K. M. (2016) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2016.01.009 · Cited by 48 · see citing works
Celiac Disease and Bone Health in Children and Adolescents: A Systematic Review and Meta-Analysis
Fedewa, M. V., Bentley, J. L., Higgins, S., Kindler, J. M., Esco, M. R., & MacDonald, H. V. (2019) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2019.02.003 · Cited by 44 · see citing works
Toward New Paradigms in the Follow Up of Adult Patients With Celiac Disease on a Gluten-Free Diet
Pinto-Sánchez, M. I., & Bai, J. C. (2019) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00153 · Cited by 43 · see citing works
Osteoporosis and Celiac Disease: Updates and Hidden Pitfalls
Lungaro, L., Manza, F., Costanzini, A., Barbalinardo, M., Gentili, D., Caputo, F., Guarino, M., Zoli, G., Volta, U., GIORGIO, R. D., et al. (2023) · Nutrients · doi:10.3390/nu15051089 · Cited by 42 · see citing works
Vitamin D and malabsorptive gastrointestinal conditions: A bidirectional relationship?
Giustina, A., di Filippo, L., Allora, A., Bikle, D. D., Cavestro, G. M., Feldman, D., Latella, G., Minisola, S., Napoli, N., Trasciatti, S., et al. (2023) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-023-09792-7 · Cited by 39 · see citing works
Walker, M. D., Williams, J. M., Lewis, S. K., Bai, J. C., Lebwohl, B., & Green, P. H. R. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2019.03.049 · Cited by 31 · see citing works
Nestares, T., Martín-Masot, R., de Teresa, C., Bonillo, R., Maldonado, J., Flor-Alemany, M., & Aparicio, V. (2021) · Nutrients · doi:10.3390/nu13051636 · Cited by 30 · see citing works
Causes of low peak bone mass in women
Chew, C. K., & Clarke, B. L. (2017) · Maturitas · doi:10.1016/j.maturitas.2017.12.010 · Cited by 29 · see citing works
Celiac disease and risk of fracture in adults—a review
Hjelle, A. M., Apalset, E. M., Mielnik, P., Bollerslev, J., Lundin, K. E. A., & Tell, G. S. (2014) · Osteoporosis International · doi:10.1007/s00198-014-2683-8 · Cited by 28 · see citing works
Bone Fragility in Gastrointestinal Disorders
Merlotti, D., Mingiano, C., Valenti, R., Cavati, G., Calabrese, M., Pirrotta, F., Bianciardi, S., Palazzuoli, A., & Gennari, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052713 · Cited by 29 · see citing works
Management of bone health in patients with celiac disease: Practical guide for clinicians.
Duerksen, D. R., Pinto-Sánchez, M. I., Anca, A., Schnetzler, J., Case, S., Zelin, J., Smallwood, A., Turner, J. M., Verdu, E. F., Butzner, J. D., et al. (2018) · Europe PMC (PubMed Central) · Cited by 27 · see citing works
Bone Density and Fractures in HIV-infected Postmenopausal Women: A Systematic Review
Cortés, Y. I., Yin, M. T., & Reame, N. K. (2015) · Journal of the Association of Nurses in AIDS Care · doi:10.1016/j.jana.2015.03.005 · Cited by 26 · see citing works
Celiac disease: Managing a multisystem disorder
Kochhar, G. S., Singh, T., Gill, A., & Kirby, D. F. (2016) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.83a.14158 · Cited by 26 · see citing works
Celiac disease: diagnosis and treatment.
Hvas, C. L., Jensen, M. D., Reimer, M., Riis, L. B., Rumessen, J. J., Skovbjerg, H., Teisner, A., & Wildt, S. (2015) · PubMed · Cited by 26 · see citing works
Wessels, M., Dolinsek, J., Castillejo, G., Donat, E., Riznik, P., Roca, M., Valitutti, F., Veenvliet, A., & Mearin, M. L. (2022) · European Journal of Pediatrics · doi:10.1007/s00431-021-04318-2 · Cited by 31 · see citing works
Celiac Disease Alone and Associated With Type 1 Diabetes Mellitus
Tsouka, A., Mahmud, F. H., & Marcon, M. A. (2015) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000789 · Cited by 30 · see citing works
Celiac Disease and Type 1 Diabetes in Adults: Is This a High-Risk Group for Screening?
DeMelo, E. N., McDonald, C. G., Saibil, F. G., MARCON, M. A., & Mahmud, F. H. (2015) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2015.06.006 · Cited by 25 · see citing works
Kondapalli, A. V., & Walker, M. D. (2022) · Archives of Endocrinology and Metabolism · doi:10.20945/2359-3997000000561 · Cited by 25 · see citing works
“In patients with normal baseline BMD, testing can be repeated in two to three years (63).”
BackgroundInfluentialDuodenal histopathology and laboratory deficiencies related to bone metabolism in coeliac disease
Posthumus, L., & Al-Toma, A. A. (2017) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000000880 · Cited by 21 · see citing works
Galli, G., Lahner, E., Conti, L., Esposito, G., Sacchi, M. C., & Annibale, B. (2018) · United European Gastroenterology Journal · doi:10.1177/2050640618784340 · Cited by 20 · see citing works
New insights into the diagnosis and management of bone health in premature ovarian insufficiency
Nguyen, H. H., Milat, F., & Vincent, A. J. (2021) · Climacteric · doi:10.1080/13697137.2021.1917539 · Cited by 20 · see citing works
Tortora, R., Imperatore, N., Capone, P., Gerbino, N., Rea, M., Affinito, G., Caporaso, N., & Rispo, A. (2017) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2017.05.010 · Cited by 13 · see citing works
Skoracka, K., Hryhorowicz, S., Tovoli, F., Raiteri, A., Rychter, A. M., Słomski, R., Dobrowolska, A., Granito, A., & Krela‐Kaźmierczak, I. (2023) · Calcified Tissue International · doi:10.1007/s00223-023-01155-3 · Cited by 12 · see citing works
Updates on bone health in children with gastrointestinal diseases
Yang, H. R. (2020) · Annals of Pediatric Endocrinology & Metabolism · doi:10.6065/apem.2020.25.1.10 · Cited by 12 · see citing works
Implementation and adherence to osteoporosis screening guidelines among coeliac disease patients
Singh, P., & Garber, J. J. (2016) · Digestive and Liver Disease · doi:10.1016/j.dld.2016.08.121 · Cited by 12 · see citing works
Celiac disease and fibromyalgia: Is there an association?
Nisihara, R., Marques, A. P., Mei, A., & Skare, T. L. (2015) · Revista Española de Enfermedades Digestivas · doi:10.17235/reed.2015.3992/2015 · Cited by 11 · see citing works
Gut-bone Cross Talks and Implications in Celiac Disease
Lerner, A., & Matthias, T. (2016) · International Journal of Celiac Disease · doi:10.12691/ijcd-4-1-4 · Cited by 11 · see citing works
Gerenlı, N., Dursun, F., Çeltık, C., & Kırmızıbekmez, H. (2020) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem-2020-0292 · Cited by 8 · see citing works
It starts from the womb: maximizing bone health
Vasanwala, R. F., Gani, L. U., & Ang, S. B. (2022) · Climacteric · doi:10.1080/13697137.2021.2011197 · Cited by 7 · see citing works
Osteoporosis in children: Possible risk factors and role of antioxidants
Sheweita, S. A., Alsamghan, A., & Khoshhal, O. (2019) · Journal of Musculoskeletal Surgery and Research · doi:10.4103/jmsr.jmsr_40_19 · Cited by 6 · see citing works
Bone and Joint Involvement in Celiac Disease
Hoffmanová, I., Sánchez, D., & Džupa, V. (2015) · Acta chirurgiae orthopaedicae et traumatologiae Cechoslovaca · doi:10.55095/achot2015/048 · Cited by 5 · see citing works
Celiac disease-related osteopathy among Saudi celiac patients: Are we adherent to recommendations?
Fouda, M. (2017) · Saudi Journal of Gastroenterology · doi:10.4103/sjg.sjg_58_17 · Cited by 5 · see citing works
Self-citationSurvey of the initial management of celiac disease antibody tests by ordering physicians
Potter, K. J., de Koning, L., Butzner, J. D., & Gidrewicz, D. (2019) · BMC Pediatrics · doi:10.1186/s12887-019-1621-5 · Cited by 4 · see citing works
Monitoring and Follow-Up of Patients with Celiac Disease
Herman, M. L., Absah, I., Oxentenko, A. S., & Rubio‐Tapia, A. (2013) · Clinical gastroenterology · doi:10.1007/978-1-4614-8560-5_12 · Cited by 3 · see citing works
Celiac Disease and its Serological Pattern in Saudi Arabia: A Systematic Review
Safi, M.-A. A., & Safi, H. M.-A. (2018) · Global Vaccines and Immunology · doi:10.15761/gvi.1000133 · Cited by 3 · see citing works
Celiac & Gluten Intolerance: A Wellness Perspective
Grace-Farfaglia, P. (2014) · Journal of Nutritional Health & Food Engineering · doi:10.15406/jnhfe.2014.01.00028 · Cited by 2 · see citing works
Dietary Supplements in Celiac Disease
Pietzak, M. M. (2013) · Clinical gastroenterology · doi:10.1007/978-1-4614-8560-5_11 · Cited by 2 · see citing works
Follow-Up of Paediatric Patients with Celiac Disease
Fernandes, A., & Lopes, A. I. (2021) · Springer eBooks · doi:10.1007/978-3-030-82401-3_10 · Cited by 2 · see citing works
Corrigendum to “Evaluation and Management of Skeletal Health in Celiac Disease: Position Statement”
Fouda, M. A., Khan, A. A., Sultan, M., Rios, L. P., McAssey, K., & Armstrong, D. (2017) · Canadian Journal of Gastroenterology and Hepatology · doi:10.1155/2017/1323607 · Cited by 2 · see citing works
Self-citationRisk Factors for Decreased Bone Density in Adults with Celiac Disease
Niknam, R., Nowrouzi, K., Mahmoudi, L., Motazedian, N., Ejtehadi, F., Boogar, S. S., & Zamani, A. (2024) · Shiraz E-Medical Journal · doi:10.5812/semj-143039 · Cited by 1 · see citing works
Shah, N., Galitzer, H., Yalamanchi, S., & Sellmeyer, D. E. (2025) · JBMR Plus · doi:10.1093/jbmrpl/ziaf089 · Cited by 1 · see citing works
Musculoskeletal consequences of coeliac disease
Migliorini, F., Simeone, F., Schäfer, L., Katusić, D., Vaishya, R., & Memminger, M. K. (2026) · European journal of medical research · doi:10.1186/s40001-026-04010-x · Cited by 1 · see citing works
Understanding the Variation in Use of Screening DXA Scans in Pediatric Patients with Celiac Disease
Webster, J., Shaw, K. N., Shea, J. A., Taylor, A., & Verma, R. (2017) · International Journal of Celiac Disease · doi:10.12691/ijcd-5-4-7 · Cited by 1 · see citing works
Bone Health in Adolescents with Chronic Disease
Sieke, E. H., & Peebles, R. (2018) · Springer eBooks · doi:10.1007/978-3-319-72880-3_11 · Cited by 1 · see citing works
SKELETAL HEALTH ASSESSMENT IN BRAZILIAN MEN WITH CELIAC DISEASE AT DIAGNOSIS: HOW IMPORTANT IS IT?
Kotze, L. M. D. S., Skare, T. L., Kotze, L. R., & Nisihara, R. (2024) · Arquivos de Gastroenterologia · doi:10.1590/s0004-2803.24612024-005 · Cited by 1 · see citing works
Walker, M. D., Lebwohl, B., & Green, P. H. R. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2019.07.048 · Cited by 1 · see citing works
Osteoporosis in Celiac Disease: An UpdatePreprint
Lungaro, L., Manza, F., Costanzini, A., Caputo, F., Zoli, G., Volta, U., GIORGIO, R. D., & Caio, G. (2022) · Preprints.org · doi:10.20944/preprints202207.0344.v1 · Cited by 1 · see citing works
Celiac Disease and Bone Health
Alaedini, A. (2014) · Springer eBooks · doi:10.1007/978-1-4939-2001-3_37
Dermatitis herpetiformis: what lies beneath the skin?
García‐Manzanares, Á., & Lucendo, A. J. (2013) · Revista Española de Enfermedades Digestivas · doi:10.4321/s1130-01082013000400001
Optimising the management of bone disease for coeliac patients in a dietetic-led clinic
Martin, K. J., & Woodall, A. (2016) · ChesterRep (University of Chester) · doi:10.12691/ijcd-4-2-6
Relationship between the Diet and the Bone Mineral Density in Children with Celiac Disease
Salazar, J. C., Espín, B., Rodriguez, A., Argüelles‐Arias, F., Garcia, R., Valverde, J., & Rubio, C. (2018) · Journal of Gastrointestinal & Digestive System · doi:10.4172/2161-069x.1000550
Duerksen, D. R., Pinto-Sánchez, M. I., Anca, A., Schnetzler, J., Case, S., Zelin, J., Smallwood, A., Turner, J. M., Verdu, E. F., Butzner, J. D., et al. (2018) · Europe PMC (PubMed Central)
Reproductive disorders, osteoporosis and secondary hyperparathyroidism with celiac disease
Krums, L. M., Владимировна, Б. С., Ea, S., Aminova, T. V., Полева, Н. И., Gudkov, R. B., Turaeva, M. B., & Parfenov, A. I. (2018) · Terapevticheskii arkhiv · doi:10.26442/terarkh201890104-93
Dehghani, S. M., Amirhakimi, A., Shahramian, I., Rahanjam, N., Fazeli, F., Hamzeloo, S., & Bidar, Z. (2020) · International journal of basic science in medicine · doi:10.34172/ijbsm.2020.06
Enfermedad celíaca y desarrollo de patologías secundarias
Solano-Sánchez, D., & Quesada-Yamasaki, D. A. (2020) · Medicina y Laboratorio · doi:10.36384/01232576.337
Moon, R. J., & Davies, J. H. (2021) · Springer eBooks · doi:10.1007/978-3-030-78128-6_12
Gluten-related disorders: monitoring and follow-up
Al-Toma, A. A., & Mulder, C. J. J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821846-4.00012-7
Celiac disease in adult patients
Ciacci, C., Micco, I. D., Stefano, M. D., & Mengoli, C. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13359-6.00001-7
Medical treatments and follow-up for clinical conditions associated to celiac disease
Gasbarrini, A., Bibbò, S., Ianiro, G., Cammarota, G., & Gasbarrini, A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13359-6.00004-2
Premenopausal women with low bone mass
Hamdy, R. C. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-99550-4.00006-x
ЦУКРОВИЙ ДІАБЕТ 1 ТИПУ ТА ЦЕЛІАКІЯ: ОГЛЯД ЛlТЕРАТУРИ
Khyzhnyak, O., Микитюк, М., Karachentsev, Y. I., Oleksyk, O. T., & Гавриш, Т. Ю. (2025) · PROBLEMS OF ENDOCRINE PATHOLOGY · doi:10.21856/j-pep.2025.3.05
Montano, A., Paolini, A., Felli, C., Bruno, S. P., Baldassarre, A., Sandal, S., & Masotti, A. (2026) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2026.1940762
- Authors
- Fouda, M. A., Khan, A. A., Sultan, M., Rios, L. P., McAssey, K., & Armstrong, D.
- Affiliations
- King Saud University (SA)
- McMaster University (CA)
- Corresponding author
- Khan, Aliya A
- Venue
- Canadian Journal of Gastroenterology
- Publisher
- Wiley
- Published
- 2012
- Volume
- 26
- Issue
- 11
- Pages
- 819-829
- ISSN
- 0835-7900 (ISSN-L)
- PMC
- PMC3495700
- OpenAlex
- W2128444812
- Cited by
- 76
- References
- 90
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 3 · 2022: 8 · 2021: 7 · 2020: 5 · 2019: 6 · 2018: 7 · 2017: 6 · 2016: 8 · 2015: 8 · 2014: 5 · 2013: 4
- FWCI
- 0.79
- Type
- journal article
- Language
- en
- Update notices
- corrigendum (2017-07-02)
- Open access
- gold
- doi.org
- Locations
- Canadian Journal of Gastroenterology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Health Sciences › Medicine › Gastroenterology › Celiac Disease Research and Management
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Pathology and Forensic Medicine › Vitamin D Research Studies
- Keywords
- celiac disease, skeletal health, osteopenia, osteoporosis, fracture risk, gluten-free diet, bone mineral density screening, antiresorptive therapy, vitamin D, parathyroid hormone, children, adults
- MeSH terms
- Adult, Age Factors, Bone Diseases, Metabolic, Celiac Disease, Child, Clinical Protocols, Female, Humans, Male, Sex Factors, Bone Density
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