Duration of Type 2 Diabetes Mellitus Over 5 Years, HbA1c Levels Over 7%, Alkaline Phospatase Over 130 IU/L, and C-Reactive Protein Over 3 mg/dL as Risk Factors for Osteoporosis in Type 2 DM Patients

Authors

  • Gede Mahardika Putra Department of Orthopedic and Traumatology, Faculty of Medicine, Udayana University, RSUP, Sanglah General Hospital, Bali, Indonesia image/svg+xml
  • Ketut Siki Kawiyana Department of Orthopedic and Traumatology, Faculty of Medicine, Udayana University, Sanglah General Hospital, Denpasar, Bali, Indonesia image/svg+xml
  • Gede Eka Wiratnaya Department of Orthopedic and Traumatology, Faculty of Medicine, Udayana University, Sanglah General Hospital, Denpasar, Bali, Indonesia image/svg+xml
  • Ketut Suyasa Department of Orthopedic and Traumatology, Faculty of Medicine, Udayana University, Sanglah General Hospital, Denpasar, Bali, Indonesia image/svg+xml

DOI:

https://doi.org/10.3889/oamjms.2023.11572

Keywords:

Diabetes mellitus, osteoporosis, duration of diabetes, hemoglobin A1c, alkaline phosphatase, c-reactive protein

Abstract

BACKGROUND: Type 2 diabetes mellitus (DM) may increases the risk of osteoporosis due to impaired osteoblast and osteoclast function, which affects the morbidity and mortality rates of DM patients. Not many studies investigating the relationship of DM with osteoporosis.

AIM: The purpose of this study was to evaluate the duration of DM, hemoglobin A1c (HbA1c), alkaline phosphatase (ALP), and C-reactive protein (CRP) levels as risk factors for osteoporosis.

METHODS: Case control study was performed on a total of 44 samples that consist of ostoporosis group and non-osteoporosis group. Difference of HbA1c, ALP, and CRP between groups was evaluated using Chi-square test.

RESULTS: Based on statistical analysis, we found that the duration of DM Type II ≥5 years (p = 0.002, odds ratio [OR] 11.08), HbA1c levels ≥7% (p = 0.027, OR 5.4), ALP ≥130 IU/L (p = 0.045, OR 5.2), and CRP ≥3 ng/dL (p = 0.033, OR 4.67) were significant risk factors for osteoporosis. Based on multivariate analysis with logistic regression, we found that risk factors for the duration of DM Type II ≥5 years had the greatest strength of association with osteoporosis.

CONCLUSION: In DM patients, duration of DM ≥5 years, HbA1c levels ≥7%, ALP ≥130 IU/L, and CRP ≥3 ng/dL are predictor factors for osteoporosis that can be used in clinical practice. These risk factors can be used as evaluation parameters for DM patients who are suspected to have osteoporosis.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Plum Analytics Artifact Widget Block

Author Biography

Ketut Siki Kawiyana, Department of Orthopedic and Traumatology, Faculty of Medicine, Udayana University, Sanglah General Hospital, Denpasar, Bali, Indonesia

Consultant, Orthopedic and Traumatology Department, Faculty of Medicine Udayana University, Sanglah General Hospital, Denpasar, Bali.

References

Kementerian Kesehatan Republik Indonesia. Profil Kesehatan Indonesia Tahun 2020. Jakarta: Kementerian Kesehatan Republik Indonesia; 2020.

Cheung CL, Ang SB, Chadha M, Chow ES, Chung YS, Hew FL, et al. An updated hip fracture projection in Asia: The Asian Federation of Osteoporosis Societies study. Osteoporos Sarcopenia. 2018;4(1):16-21. https://doi.org/10.1016/j.afos.2018.03.003 PMid:30775536 DOI: https://doi.org/10.1016/j.afos.2018.03.003

Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 2022;183:109119. https://doi.org/10.1016/j.diabres.2021.109119 PMid:34879977 DOI: https://doi.org/10.1016/j.diabres.2021.109119

Kementerian Kesehatan RI. Riset Kesehatan Dasar 2018. Indonesia: Kementerian Kesehatan RI; 2018.

Leidig-Bruckner G, Ziegler R. Diabetes mellitus a risk for osteoporosis? Exp Clin Endocrinol Diabetes. 2001;109 Suppl 2:S493-514. https://doi.org/10.1055/s-2001-18605 PMid:11460594 DOI: https://doi.org/10.1055/s-2001-18605

Montagnani A, Gonnelli S, Alessandri M, Nuti R. Osteoporosis and risk of fracture in patients with diabetes: An update. Aging Clin Exp Res. 2011;23(2):84-90. https://doi.org/10.1007/BF03351073 PMid:21743287 DOI: https://doi.org/10.1007/BF03351073

Raška I Jr., Rašková M, Zikán V, Škrha J. Prevalence and risk factors of osteoporosis in postmenopausal women with Type 2 diabetes mellitus. Cent Eur J Public Health. 2017;25(1):3-10. https://doi.org/10.21101/cejph.a4717 PMid:28399348 DOI: https://doi.org/10.21101/cejph.a4717

Li KH, Liu YT, Yang YW, Lin YL, Hung ML, Lin IC. A positive correlation between blood glucose level and bone mineral density in Taiwan. Arch Osteoporos. 2018;13(1):78. https://doi.org/10.1007/s11657-018-0494-9 PMid:30009330 DOI: https://doi.org/10.1007/s11657-018-0494-9

Chen H, Li J, Wang Q. Associations between bone-alkaline phosphatase and bone mineral density in adults with and without diabetes. Medicine (Baltimore). 2018;97(17):e0432. https://doi.org/10.1097/MD.0000000000010432 PMid:29702995 DOI: https://doi.org/10.1097/MD.0000000000010432

Jang M, Kim H, Lea S, Oh S, Kim JS, Oh B. Effect of duration of diabetes on bone mineral density: A population study on East Asian males. BMC Endocr Disord. 2018;18(1):61. https://doi.org/10.1186/s12902-018-0290-y PMid:30185190 DOI: https://doi.org/10.1186/s12902-018-0290-y

Nicodemus KK, Folsom AR, Iowa Women’s Health Study. Type 1 and Type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24(7):1192-7. https://doi.org/10.2337/diacare.24.7.1192 PMid:11423501 DOI: https://doi.org/10.2337/diacare.24.7.1192

Ivers RQ, Cumming RG, Mitchell P, Peduto AJ, Blue Mountains Eye Study. Diabetes and risk of fracture: The blue mountains eye study. Diabetes Care. 2001;24(7):1198-203. https://doi.org/10.2337/diacare.24.7.1198 PMid:11423502 DOI: https://doi.org/10.2337/diacare.24.7.1198

Brown SA, Sharpless JL. Osteoporosis: An Under-appreciated complication of diabetes. Clin Diabetes. 2004;22(1):10-20. https://doi.org/10.2337/diaclin.22.1.10 DOI: https://doi.org/10.2337/diaclin.22.1.10

Goldshtein I, Nguyen AM, dePapp AE, Ish-Shalom S, Chandler JM, Chodick G, et al. Epidemiology and correlates of osteoporotic fractures among Type 2 diabetic patients. Arch Osteoporos. 2018;13(1):15. https://doi.org/10.1007/s11657-018-0432-x PMid:29502187 DOI: https://doi.org/10.1007/s11657-018-0432-x

Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with Type 1 and Type 2 diabetes--a meta-analysis. Osteoporos Int. 2007;18(4):427-44. https://doi.org/10.1007/s00198-006-0253-4 PMid:17068657 DOI: https://doi.org/10.1007/s00198-006-0253-4

Leidig-Bruckner G, Grobholz S, Bruckner T, Scheidt-Nave C, Nawroth P, Schneider JG. Prevalence and determinants of osteoporosis in patients with Type 1 and Type 2 diabetes mellitus. BMC Endocr Disord. 2014;14:33. https://doi.org/10.1186/1472-6823-14-33 PMid:24721668 DOI: https://doi.org/10.1186/1472-6823-14-33

Anaforoglu I, Nar-Demirer A, Bascil-Tutuncu N, Ertorer ME. Prevalence of osteoporosis and factors affecting bone mineral density among postmenopausal Turkish women with Type 2 diabetes. J Diabetes Complications. 2009;23(1):12-7. https://doi.org/10.1016/j.jdiacomp.2007.06.004 PMid:18413190 DOI: https://doi.org/10.1016/j.jdiacomp.2007.06.004

Murray CE, Coleman CM. Impact of diabetes mellitus on bone health. Int J Mol Sci. 2019;20(19):4873. https://doi.org/10.3390/ijms20194873 PMid:31575077 DOI: https://doi.org/10.3390/ijms20194873

Lin HH, Hsu HY, Tsai MC, Hsu LY, Chien KL, Yeh TL. Association between Type 2 diabetes and osteoporosis risk: A representative cohort study in Taiwan. PLoS One. 2021;16(7):e0254451. https://doi.org/10.1371/journal.pone.0254451 PMid:34255803 DOI: https://doi.org/10.1371/journal.pone.0254451

Oei L, Zillikens MC, Dehghan A, Buitendijk GH, Castaño- Betancourt MC, Estrada K, et al. High bone mineral density and fracture risk in Type 2 diabetes as skeletal complications of inadequate glucose control: The Rotterdam Study. Diabetes Care. 2013;36(6):1619-28. https://doi.org/10.2337/dc12-1188 PMid:23315602 DOI: https://doi.org/10.2337/dc12-1188

Garg R, Chen Z, Beck T, Cauley JA, Wu G, Nelson D, et al. Hip geometry in diabetic women: Implications for fracture risk. Metabolism. 2012;61(12):1756-62. https://doi.org/10.1016/j.metabol.2012.05.010 PMid:22726843 DOI: https://doi.org/10.1016/j.metabol.2012.05.010

Melton LJ 3rd, Leibson CL, Achenbach SJ, Therneau TM, Khosla S. Fracture risk in Type 2 diabetes: Update of a population- based study. J Bone Miner Res. 2008;23(8):1334-42. https://doi.org/10.1359/jbmr.080323 PMid:18348689 DOI: https://doi.org/10.1359/jbmr.080323

Bandeira F, Costa AG, Soares Filho MA, Pimentel L, Lima L, Bilezikian JP. Bone markers and osteoporosis therapy. Arq Bras Endocrinol Metabol. 2014;58(5):504-13. https://doi.org/10.1590/0004-2730000003384 PMid:25166041 DOI: https://doi.org/10.1590/0004-2730000003384

Park JC, Kovesdy CP, Duong U, Streja E, Rambod M, Nissenson AR, et al. Association of serum alkaline phosphatase and bone mineral density in maintenance hemodialysis patients. Hemodial Int. 2010;14(2):182-92. https://doi.org/10.1111/j.1542-4758.2009.00430.x DOI: https://doi.org/10.1111/j.1542-4758.2009.00430.x

Kang KY, Hong YS, Park SH, Ju JH. Increased serum alkaline phosphatase levels correlate with high disease activity and low bone mineral density in patients with axial spondyloarthritis. Semin Arthritis Rheum. 2015;45(2):202-7. https://doi.org/10.1016/j.semarthrit.2015.03.002 PMid:25895696 DOI: https://doi.org/10.1016/j.semarthrit.2015.03.002

Lumachi F, Orlando R, Fallo F, Basso SM. Relationship between bone formation markers bone alkaline phosphatase, osteocalcin and amino-terminal propeptide of Type I collagen and bone mineral density in elderly men. Preliminary results. In vivo. 2012;26(6):1041-4.

Malluche HH, Davenport DL, Cantor T, Monier-Faugere MC. Bone mineral density and serum biochemical predictors of bone loss in patients with CKD on dialysis. Clin J Am Soc Nephrol. 2014;9(7):1254-62. https://doi.org/10.2215/CJN.09470913 PMid:24948144 DOI: https://doi.org/10.2215/CJN.09470913

Chen Z, Zhao GH, Zhang YK, Shen GS, Xu YJ, Xu NW. Research on the correlation of diabetes mellitus complicated with osteoporosis with lipid metabolism, adipokines and inflammatory factors and its regression analysis. Eur Rev Med Pharmacol Sci. 2017;21(17):3900-5.

Mitama Y, Fujiwara S, Yoneda M, Kira S, Kohno N. Association of Type 2 diabetes and an inflammatory marker with incident bone fracture among a Japanese cohort. J Diabetes Investig. 2017;8(5):709-15. https://doi.org/10.1111/jdi.12632 PMid:28122172 DOI: https://doi.org/10.1111/jdi.12632

Ishii S, Cauley JA, Greendale GA, Crandall CJ, Danielson ME, Ouchi Y, et al. C-reactive protein, bone strength, and nine-year fracture risk: Data from the Study of Women’s Health Across the Nation (SWAN). J Bone Miner Res. 2013;28(7):1688-98. https://doi.org/10.1002/jbmr.1915 PMid:23456822 DOI: https://doi.org/10.1002/jbmr.1915

Schett G, Kiechl S, Weger S, Pederiva A, Mayr A, Petrangeli M, et al. High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch Intern Med. 2006;166(22):2495-501. https://doi.org/10.1001/archinte.166.22.2495 PMid:17159016 DOI: https://doi.org/10.1001/archinte.166.22.2495

Berglundh S, Malmgren L, Luthman H, McGuigan F, Åkesson K. C-reactive protein, bone loss, fracture, and mortality in elderly women: A longitudinal study in the OPRA cohort. Osteoporos Int. 2015;26(2):727-35. https://doi.org/10.1007/s00198-014-2951-7 PMid:25410434 DOI: https://doi.org/10.1007/s00198-014-2951-7

Bhupathiraju SN, Alekel DL, Stewart JW, Hanson LN, Shedd KM, Reddy MB, et al. Relationship of circulating total homocysteine and C-reactive protein to trabecular bone in postmenopausal women. J Clin Densitom. 2007;10(4):395-403. https://doi.org/10.1016/j.jocd.2007.06.002 PMid:17662632 DOI: https://doi.org/10.1016/j.jocd.2007.06.002

Pasco JA, Kotowicz MA, Henry MJ, Nicholson GC, Spilsbury HJ, Box JD, et al. High-sensitivity C-reactive protein and fracture risk in elderly women. JAMA. 2006;296(11):1353-5. https://doi.org/10.1001/jama.296.11.1353 PMid:16985226 DOI: https://doi.org/10.1001/jama.296.11.1353

Nakamura K, Saito T, Kobayashi R, Oshiki R, Oyama M, Nishiwaki T, et al. C-reactive protein predicts incident fracture in community-dwelling elderly Japanese women: The Muramatsu study. Osteoporos Int. 2011;22(7):2145-50. https://doi.org/10.1007/s00198-010-1425-9 PMid:20936400 DOI: https://doi.org/10.1007/s00198-010-1425-9

Ganesan K, Teklehaimanot S, Tran TH, Asuncion M, Norris K. Relationship of C-reactive protein and bone mineral density in community-dwelling elderly females. J Natl Med Assoc 2005;97(3):329-33.

Downloads

Published

2023-09-01

How to Cite

1.
Putra GM, Kawiyana KS, Wiratnaya GE, Suyasa K. Duration of Type 2 Diabetes Mellitus Over 5 Years, HbA1c Levels Over 7%, Alkaline Phospatase Over 130 IU/L, and C-Reactive Protein Over 3 mg/dL as Risk Factors for Osteoporosis in Type 2 DM Patients. Open Access Maced J Med Sci [Internet]. 2023 Sep. 1 [cited 2024 May 3];11(B):714-9. Available from: https://oamjms.eu/index.php/mjms/article/view/11572