Research Article
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Evaluation of Osteoporosis and Associated Factors in Patients with Type 1 Diabetes Mellitus

Year 2025, Volume: 15 Issue: 1, 47 - 58
https://doi.org/10.31832/smj.1598017

Abstract

Objective: This paper aims to assess the prevalence of osteoporosis in patients with T1DM by studying the influence of the main risk factors: BMI, calcium intake, vitamin D, lactose intolerance, and BMD, along with the risk of fractures.
Material and Methods: Cross-sectional study in 30 patients with T1DM and 30 normal controls. BMD was measured using DEXA, further calculating BMI, daily calcium intake, and vitamin D levels. Osteoporosis and fracture risk were evaluated by statistical analysis using the data obtained.
Results: Patients with T1DM had lower BMI (p < 0.001), lower daily calcium intake (p < 0.001), and lower L1-L4 Z scores (p = 0.002) compared to controls. High HbA1c was significantly associated with an increased risk of hip fracture (OR = 1.58, p = 0.022), and low BMI was also a crucial predictor of increased risk of fracture (OR = 1.49, p = 0.012) and osteoporosis (OR = 1.29, p = 0.018). It could be seen that lactose intolerance and calcium deficiency considerably increased the risk of osteoporosis and fractures.
Conclusion: Our study underlines the pivotal role of BMI, calcium intake, and lactose intolerance in determining osteoporosis and fracture risk in T1DM patients. Our findings emphasize once more how managing these risk factors by specific interventions may play a key role in preventing osteoporosis and fractures.

References

  • Kurra S, Siris E (2011) Diabetes and bone health: The relationship between diabetes and osteoporosis‐associated fractures. Diabetes/Metabolism Research and Reviews 27:430-435. https://doi.org/10.1002/dmrr.1197
  • (WHO) WHO (2023) Prevalence of diabetes and related factors [Internet]. Accessed Date Accessed 2023 Accessed
  • Gagnum V, Saeed M, Stene LC, Leivestad T, Joner G, Skrivarhaug T (2018) Low Incidence of End-Stage Renal Disease in Childhood-Onset Type 1 Diabetes Followed for Up to 42 Years. Diabetes Care 41:420-425. https://doi.org/10.2337/dc17-0906
  • Atkinson MA, Eisenbarth GS, Michels AW (2014) Type 1 diabetes. The Lancet 383:69-82. https://doi.org/10.1016/s0140-6736(13)60591-7
  • Leungsuwan DS, Chandran M. Bone Fragility in Diabetes and its Management: A Narrative Review. Drugs. 2024 Sep;84(9):1111-1134. doi: 10.1007/s40265-024-02078-5.
  • Mohsin F, Craig ME, Cusumano J, Chan AKF, Hing S, Lee JW, Silink M, Howard NJ, Donaghue KC (2005) Discordant Trends in Microvascular Complications in Adolescents With Type 1 Diabetes From 1990 to 2002. Diabetes Care 28:1974-1980. https://doi.org/10.2337/diacare.28.8.1974
  • Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and Economic Burden of Osteoporosis-Related Fractures in the United States, 2005–2025. Journal of Bone and Mineral Research 22:465-475. https://doi.org/10.1359/jbmr.061113
  • Harvey N, Dennison E, Cooper C (2010) Osteoporosis: Impact on health and economics. Nature Reviews Rheumatology 6:99-105. https://doi.org/10.1038/nrrheum.2009.260
  • Salari N, Ghasemi H, Mohammadi L, Behzadi Mh, Rabieenia E, Shohaimi S, Mohammadi M (2021) The global prevalence of osteoporosis worldwide: A comprehensive systematic review and meta-analysis. Journal of Orthopaedic Surgery and Research 16. https://doi.org/10.1186/s13018-021-02772-0
  • Saito M, Marumo K (2009) Collagen cross-links as a determinant of bone quality: A possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporosis International 21:195-214. https://doi.org/10.1007/s00198-009-1066-z
  • Zhukouskaya VV, Eller-Vainicher C, Shepelkevich AP, Dydyshko Y, Cairoli E, Chiodini I (2015) Bone health in type 1 diabetes: Focus on evaluation and treatment in clinical practice. Journal of Endocrinological Investigation 38:941-950. https://doi.org/10.1007/s40618-015-0284-9
  • Valerio G, del Puente A, Esposito-del Puente A, Buono P, Mozzillo E, Franzese A (2002) The Lumbar Bone Mineral Density is Affected by Long-Term Poor Metabolic Control in Adolescents with Type 1 Diabetes mellitus. Hormone Research in Paediatrics 58:266-272. https://doi.org/10.1159/000066441
  • American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of Medical Care in Diabetesd2018. Diabetes Care 2018;41(Suppl. 1):S13–S27.
  • Forlenza GP, Rewers M (2011) The epidemic of type 1 diabetes. Current Opinion in Endocrinology, Diabetes and Obesity 18:248-251. https://doi.org/10.1097/MED.0b013e32834872ce
  • Cosman F, Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R. Clinician’s Guide to Prevention and Treatment of Osteoporosis. Osteoporos Int 2014;25:2359-2381
  • Harjutsalo V, Sund R, Knip M, Groop P-H (2013) Incidence of Type 1 Diabetes in Finland. Jama 310. https://doi.org/10.1001/jama.2013.8399
  • (IDF). IDF (2023) Type 1 Diabetes [İnternet]. Accessed Date Accessed 2023 Accessed
  • Roggen I, Gies I, Vanbesien J, Louis O, De Schepper J (2013) Trabecular Bone Mineral Density and Bone Geometry of the Distal Radius at Completion of Pubertal Growth in Childhood Type 1 Diabetes. Hormone Research in Paediatrics 79:68-74. https://doi.org/10.1159/000346686
  • Moerman EJ, Teng K, Lipschitz DA, Lecka‐Czernik B (2004) Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: The role of PPAR‐γ2 transcription factor and TGF‐β/BMP signaling pathways. Aging Cell 3:379-389. https://doi.org/10.1111/j.1474-9728.2004.00127.x
  • (1993) The Effect of Intensive Diabetes Treatment on the Development and Progression of Long-Term Complications in Insulin-Dependent Diabetes Mellitus. New England Journal of Medicine 329:977-986. https://doi.org/10.1056/nejm199309303291401
  • Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F (2011) Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. Journal of Diabetes and its Complications 25:216-221. https://doi.org/10.1016/j.jdiacomp.2011.02.004
  • Gunczler P, Lanes R, Paoli M, Martinis R, Villaroel O, Weisinger JR (2001) Decreased Bone Mineral Density and Bone Formation Markers Shortly After Diagnosis of Clinical Type 1 Diabetes Mellitus. Journal of Pediatric Endocrinology and Metabolism 14. https://doi.org/10.1515/jpem.2001.14.5.525
  • Vestergaard P (2006) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporosis International 18:427-444. https://doi.org/10.1007/s00198-006-0253-4
  • Joshi A, Varthakavi P, Chadha M, Bhagwat N (2013) A Study of Bone Mineral Density and Its Determinants in Type 1 Diabetes Mellitus. Journal of Osteoporosis 2013:1-8. https://doi.org/10.1155/2013/397814
  • Heilman K, Zilmer M, Zilmer K, Tillmann V (2009) Lower bone mineral density in children with type 1 diabetes is associated with poor glycemic control and higher serum ICAM-1 and urinary isoprostane levels. Journal of Bone and Mineral Metabolism 27:598-604. https://doi.org/10.1007/s00774-009-0076-4
  • Brandao FR, Vicente EJ, Daltro CH, Sacramento M, Moreira A, Adan L. Bone metabolism is linked to disease duration and metabolic control in type 1 diabetes mellitus. Diabetes Res Clin Pract. 2007 Dec;78(3):334-9. doi: 10.1016/j.diabres.2007.04.009.
  • Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in Patients With Diabetes Mellitus. Journal of Bone and Mineral Research 22:1317-1328. https://doi.org/10.1359/jbmr.070510
  • Bridges MJ, Moochhala SH, Barbour J, Kelly CA (2005) Influence of diabetes on peripheral bone mineral density in men: A controlled study. Acta Diabetologica 42:82-86. https://doi.org/10.1007/s00592-005-0183-1
  • Tuominen JT, Impivaara O, Puukka P, Ronnemaa T 1999 Bone mineral density in patients with type 1 and 2 diabetes. Diabetes Care 22: 1196–1200.
  • Rix M, Andreassen H, Eskildsen P (1999) Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22:827-831. https://doi.org/10.2337/diacare.22.5.827
  • Bouillon R (1991) Diabetic bone disease. Calcified Tissue International 49:155-160. https://doi.org/10.1007/bf02556109
  • Eller-Vainicher C, Zhukouskaya VV, Tolkachev YV, Koritko SS, Cairoli E, Grossi E, Beck-Peccoz P, Chiodini I, Shepelkevich AP (2011) Low Bone Mineral Density and Its Predictors in Type 1 Diabetic Patients Evaluated by the Classic Statistics and Artificial Neural Network Analysis. Diabetes Care 34:2186-2191. https://doi.org/10.2337/dc11-0764
  • Wierzbicka E, Szalecki M, Pludowski P, Jaworski M, Brzozowska A (2016) Vitamin D status, body composition and glycemic control in Polish adolescents with type 1 diabetes. Minerva Endocrinol 41:445-455
  • Michaëlsson K, Bergström R, Holmberg L, Mallmin H, Wolk A, Ljunghall S (1997) A high dietary calcium intake is needed for a positive effect on bone density in Swedish postmenopausal women. Osteoporosis International 7:155-161. https://doi.org/10.1007/bf01623692
  • Maggio ABR, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ (2010) Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. Journal of Pediatric Endocrinology and Metabolism 23. https://doi.org/10.1515/jpem.2010.23.7.697
  • Honkanen R, Pulkkinen P, Järvinen R, Kröger H, Lindstedt K, Tuppurainen M, Uusitupa M (1996) Does lactose intolerance predispose to low bone density? A population-based study of perimenopausal finnish women. Bone 19:23-28. https://doi.org/10.1016/8756-3282(96)00107-x

Tip 1 Diyabetli Hastalarda Osteoporoz ve İlişkili Faktörlerin Değerlendirilmesi

Year 2025, Volume: 15 Issue: 1, 47 - 58
https://doi.org/10.31832/smj.1598017

Abstract

Amaç: Bu araştırmanın amacı T1DM'li hastalarda osteoporoz prevalansını değerlendirmek ve vücut kitle indeksi, günlük kalsiyum alımı, D vitamini düzeyi ve laktoz intoleransının kırık riski ile ilişkisinin değerlendirilmesidir.
Materyal ve Method: Araştırma 30 T1DM'li hasta ve 30 diyabet tanısı olmayan bireylerin değerlendirildiği kesitsel bir çalışmadır. Çalışmaya katılan hastaların kemik yoğunluk ölçümleri DEXA yöntemi kullanılarak ölçüldü ve VKİ, günlük kalsiyum alımı ile D vitamini seviyeleri hesaplandı. Elde edilen veriler ile istatistiksel analizler yapılarak osteoporoz ve kırık riski değerlendirildi.
Bulgular: T1DM'li hastalar kontrollerle karşılaştırıldığında daha düşük VKİ (p < 0,001), daha düşük günlük kalsiyum alımı (p < 0,001) ve daha düşük L1-L4 Z skorları (p = 0,002) saptandı. Yüksek HbA1c kalça kırığı riskinin artmasıyla önemli ölçüde ilişkiliydi (OR = 1,58, p = 0,022) ve düşük VKİ artmış kırık riskinin (OR = 1,49, p = 0,012) ve osteoporozun (OR = 1,29, p = 0,018) önemli bir belirteciydi. Laktoz intoleransı ve kalsiyum eksikliğinin osteoporoz ve kırık riskini önemli ölçüde artırdığı saptandı.
Sonuç: Çalışmamız, T1DM hastalarında osteoporoz ve kırık riskini belirlemede VKİ, günlük kalsiyum alımı ve laktoz intoleransının temel rolünü vurgulamaktadır. Bulgularımız, bu risk faktörlerinin belirli müdahalelerle yönetilmesinin osteoporoz ve kırıkların önlenmesinde nasıl önemli bir rol oynayabileceğini bir kez daha vurgulamaktadır.

References

  • Kurra S, Siris E (2011) Diabetes and bone health: The relationship between diabetes and osteoporosis‐associated fractures. Diabetes/Metabolism Research and Reviews 27:430-435. https://doi.org/10.1002/dmrr.1197
  • (WHO) WHO (2023) Prevalence of diabetes and related factors [Internet]. Accessed Date Accessed 2023 Accessed
  • Gagnum V, Saeed M, Stene LC, Leivestad T, Joner G, Skrivarhaug T (2018) Low Incidence of End-Stage Renal Disease in Childhood-Onset Type 1 Diabetes Followed for Up to 42 Years. Diabetes Care 41:420-425. https://doi.org/10.2337/dc17-0906
  • Atkinson MA, Eisenbarth GS, Michels AW (2014) Type 1 diabetes. The Lancet 383:69-82. https://doi.org/10.1016/s0140-6736(13)60591-7
  • Leungsuwan DS, Chandran M. Bone Fragility in Diabetes and its Management: A Narrative Review. Drugs. 2024 Sep;84(9):1111-1134. doi: 10.1007/s40265-024-02078-5.
  • Mohsin F, Craig ME, Cusumano J, Chan AKF, Hing S, Lee JW, Silink M, Howard NJ, Donaghue KC (2005) Discordant Trends in Microvascular Complications in Adolescents With Type 1 Diabetes From 1990 to 2002. Diabetes Care 28:1974-1980. https://doi.org/10.2337/diacare.28.8.1974
  • Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and Economic Burden of Osteoporosis-Related Fractures in the United States, 2005–2025. Journal of Bone and Mineral Research 22:465-475. https://doi.org/10.1359/jbmr.061113
  • Harvey N, Dennison E, Cooper C (2010) Osteoporosis: Impact on health and economics. Nature Reviews Rheumatology 6:99-105. https://doi.org/10.1038/nrrheum.2009.260
  • Salari N, Ghasemi H, Mohammadi L, Behzadi Mh, Rabieenia E, Shohaimi S, Mohammadi M (2021) The global prevalence of osteoporosis worldwide: A comprehensive systematic review and meta-analysis. Journal of Orthopaedic Surgery and Research 16. https://doi.org/10.1186/s13018-021-02772-0
  • Saito M, Marumo K (2009) Collagen cross-links as a determinant of bone quality: A possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporosis International 21:195-214. https://doi.org/10.1007/s00198-009-1066-z
  • Zhukouskaya VV, Eller-Vainicher C, Shepelkevich AP, Dydyshko Y, Cairoli E, Chiodini I (2015) Bone health in type 1 diabetes: Focus on evaluation and treatment in clinical practice. Journal of Endocrinological Investigation 38:941-950. https://doi.org/10.1007/s40618-015-0284-9
  • Valerio G, del Puente A, Esposito-del Puente A, Buono P, Mozzillo E, Franzese A (2002) The Lumbar Bone Mineral Density is Affected by Long-Term Poor Metabolic Control in Adolescents with Type 1 Diabetes mellitus. Hormone Research in Paediatrics 58:266-272. https://doi.org/10.1159/000066441
  • American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of Medical Care in Diabetesd2018. Diabetes Care 2018;41(Suppl. 1):S13–S27.
  • Forlenza GP, Rewers M (2011) The epidemic of type 1 diabetes. Current Opinion in Endocrinology, Diabetes and Obesity 18:248-251. https://doi.org/10.1097/MED.0b013e32834872ce
  • Cosman F, Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R. Clinician’s Guide to Prevention and Treatment of Osteoporosis. Osteoporos Int 2014;25:2359-2381
  • Harjutsalo V, Sund R, Knip M, Groop P-H (2013) Incidence of Type 1 Diabetes in Finland. Jama 310. https://doi.org/10.1001/jama.2013.8399
  • (IDF). IDF (2023) Type 1 Diabetes [İnternet]. Accessed Date Accessed 2023 Accessed
  • Roggen I, Gies I, Vanbesien J, Louis O, De Schepper J (2013) Trabecular Bone Mineral Density and Bone Geometry of the Distal Radius at Completion of Pubertal Growth in Childhood Type 1 Diabetes. Hormone Research in Paediatrics 79:68-74. https://doi.org/10.1159/000346686
  • Moerman EJ, Teng K, Lipschitz DA, Lecka‐Czernik B (2004) Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: The role of PPAR‐γ2 transcription factor and TGF‐β/BMP signaling pathways. Aging Cell 3:379-389. https://doi.org/10.1111/j.1474-9728.2004.00127.x
  • (1993) The Effect of Intensive Diabetes Treatment on the Development and Progression of Long-Term Complications in Insulin-Dependent Diabetes Mellitus. New England Journal of Medicine 329:977-986. https://doi.org/10.1056/nejm199309303291401
  • Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F (2011) Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. Journal of Diabetes and its Complications 25:216-221. https://doi.org/10.1016/j.jdiacomp.2011.02.004
  • Gunczler P, Lanes R, Paoli M, Martinis R, Villaroel O, Weisinger JR (2001) Decreased Bone Mineral Density and Bone Formation Markers Shortly After Diagnosis of Clinical Type 1 Diabetes Mellitus. Journal of Pediatric Endocrinology and Metabolism 14. https://doi.org/10.1515/jpem.2001.14.5.525
  • Vestergaard P (2006) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporosis International 18:427-444. https://doi.org/10.1007/s00198-006-0253-4
  • Joshi A, Varthakavi P, Chadha M, Bhagwat N (2013) A Study of Bone Mineral Density and Its Determinants in Type 1 Diabetes Mellitus. Journal of Osteoporosis 2013:1-8. https://doi.org/10.1155/2013/397814
  • Heilman K, Zilmer M, Zilmer K, Tillmann V (2009) Lower bone mineral density in children with type 1 diabetes is associated with poor glycemic control and higher serum ICAM-1 and urinary isoprostane levels. Journal of Bone and Mineral Metabolism 27:598-604. https://doi.org/10.1007/s00774-009-0076-4
  • Brandao FR, Vicente EJ, Daltro CH, Sacramento M, Moreira A, Adan L. Bone metabolism is linked to disease duration and metabolic control in type 1 diabetes mellitus. Diabetes Res Clin Pract. 2007 Dec;78(3):334-9. doi: 10.1016/j.diabres.2007.04.009.
  • Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in Patients With Diabetes Mellitus. Journal of Bone and Mineral Research 22:1317-1328. https://doi.org/10.1359/jbmr.070510
  • Bridges MJ, Moochhala SH, Barbour J, Kelly CA (2005) Influence of diabetes on peripheral bone mineral density in men: A controlled study. Acta Diabetologica 42:82-86. https://doi.org/10.1007/s00592-005-0183-1
  • Tuominen JT, Impivaara O, Puukka P, Ronnemaa T 1999 Bone mineral density in patients with type 1 and 2 diabetes. Diabetes Care 22: 1196–1200.
  • Rix M, Andreassen H, Eskildsen P (1999) Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22:827-831. https://doi.org/10.2337/diacare.22.5.827
  • Bouillon R (1991) Diabetic bone disease. Calcified Tissue International 49:155-160. https://doi.org/10.1007/bf02556109
  • Eller-Vainicher C, Zhukouskaya VV, Tolkachev YV, Koritko SS, Cairoli E, Grossi E, Beck-Peccoz P, Chiodini I, Shepelkevich AP (2011) Low Bone Mineral Density and Its Predictors in Type 1 Diabetic Patients Evaluated by the Classic Statistics and Artificial Neural Network Analysis. Diabetes Care 34:2186-2191. https://doi.org/10.2337/dc11-0764
  • Wierzbicka E, Szalecki M, Pludowski P, Jaworski M, Brzozowska A (2016) Vitamin D status, body composition and glycemic control in Polish adolescents with type 1 diabetes. Minerva Endocrinol 41:445-455
  • Michaëlsson K, Bergström R, Holmberg L, Mallmin H, Wolk A, Ljunghall S (1997) A high dietary calcium intake is needed for a positive effect on bone density in Swedish postmenopausal women. Osteoporosis International 7:155-161. https://doi.org/10.1007/bf01623692
  • Maggio ABR, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ (2010) Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. Journal of Pediatric Endocrinology and Metabolism 23. https://doi.org/10.1515/jpem.2010.23.7.697
  • Honkanen R, Pulkkinen P, Järvinen R, Kröger H, Lindstedt K, Tuppurainen M, Uusitupa M (1996) Does lactose intolerance predispose to low bone density? A population-based study of perimenopausal finnish women. Bone 19:23-28. https://doi.org/10.1016/8756-3282(96)00107-x
There are 36 citations in total.

Details

Primary Language English
Subjects ​Internal Diseases
Journal Section Research Article
Authors

Nazif Yalçın 0000-0002-0110-0498

Türkan Paşalı Kilit 0000-0003-1126-7336

Kevser Onbaşı 0000-0003-2230-9263

Nizameddin Koca 0000-0003-1457-4366

Early Pub Date March 25, 2025
Publication Date
Submission Date December 7, 2024
Acceptance Date March 3, 2025
Published in Issue Year 2025 Volume: 15 Issue: 1

Cite

AMA Yalçın N, Paşalı Kilit T, Onbaşı K, Koca N. Evaluation of Osteoporosis and Associated Factors in Patients with Type 1 Diabetes Mellitus. Sakarya Tıp Dergisi. March 2025;15(1):47-58. doi:10.31832/smj.1598017

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